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THE

TEXAS JOURNAL

SCIENCE

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THE TEXAS JOURNAL OF SCIENCE

Volume 56, No. 1

February, 2004

CONTENTS

Growth and Survival of Juniperus ashei (Cupressacae) Seedlings in the
Presence of Juniperus ashei Litter.

By Duncan McKinley and O. W. Van Auken . 3

The Vascular Flora of the Palo Alto National Battlefield Historic Site,

Cameron County, Texas.

By Robert I. Lonard, Alfred T. Richardson

and N. L. Richard . 15

Spatial and Temporal Abiotic Changes along a Canopy to Intercanopy Gradient
in Central Texas Juniperus ashei Woodlands.

By Rob Wayne and O. W. Van Auken . 35

Reproductive Cycle of the Sidewinder, Crotalus cerastes (Serpentes: Viperidae),
from California.

By Stephen R. Goldberg . 55

Freshwater Mussels (Bivalvia: Unionidae) of the Village Creek Drainage Basin
in Southeast Texas.

By Vickie L. Bordelon and Richard C. Harrel . 63

General Notes

Noteworthy Records of the Millipeds, Eurymerodesmus angularis and
E. mundus (Polydesmida: Eurymerodesmidae), from Northeastern and
Westcentral Texas.

By Chris T. McAllister, Rowland M. Shelley

and Dawn /. Moore . 73

Diet of the White-collared Seedeater Sporophila torqueola
(Passeriformes: Emberizidae) in Texas.

By Jack C. Eitniear . 77

Reproduction in the Coffee Snake, Ninia maculata (Serpentes: Colubridae),
from Costa Rica.

By Stephen R. Goldberg . 81

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Associate Editor for Environmental Science:

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Associate Editor for Geology:

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AFFILIATED ORGANIZATIONS
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TEXAS J. SCI. 56(1):3-14

FEBRUARY, 2004

GROWTH AND SURVIVAL OF
JUNIPERUS ASHE1 (CUPRESSACAE) SEEDLINGS
IN THE PRESENCE OF JUNIPERUS ASHE1 LITTER

Duncan McKinley* and O. W. Van Auken

Department of Biology
The University of Texas at San Antonio
6900 North Loop 1604 West
San Antonio Texas, 78249-0661
* Current address:

Division of Biology
Kansas State University
Manhattan, Kansas 66506

Abstract.— A greenhouse experiment was conducted to determine the effect of Juniperus
ashei litter on the growth and survival of J. ashei seedlings. Incremental additions (0-250
g) of J. ashei tree litter or vermiculite (control) were placed on 15 by 15 cm pots, which
contained transplanted J. ashei seedlings in 800 g of mineral soil. There were no significant
differences in the mean absolute differences in growth of J. ashei seedling considering basal
diameter, seedling height and number of branches between the J. ashei tree litter additions
and the vermiculite additions, or the amounts of both types of litter. However, there were
non-significant positive increases in the seedling growth in the 50 g treatment of both litter
types followed by a decrease at higher levels. Mortalities were highest at greater levels of
both types of litter, but were still non-significant. The responses of the J. ashei seedlings
with respect to growth and survival in the J. ashei litter and vermiculite suggest that there
is no allelopathic component in the J. ashei litter affecting seedling growth and survival or
if there is, it is transient.

Juniperus ashei is an evergreen, aromatic, dioecious, non-sprouting
shrub or small tree (Correll & Johnston 1979). It is usually found on
calcareous, rocky, shallow soils from southern Missouri and northern
Arkansas through Oklahoma, Texas and parts of northern Mexico (Little
1979; Simpson 1988; Hart & Price 1990; Fuhlendorf et al. 1997).
Fourteen species of Juniperus have been identified in North America
(Little 1979), with over 60 species found worldwide, mostly in semi-arid
northern hemisphere ecosystems (Dallimore & Jackson 1967). Various
species of Juniperus now cover approximately 10 million hectares in
Texas (Gould 1969). Juniperus ashei is a dominant species of many
savannahs and woodlands of the Edwards Plateau of central Texas (Van
Auken et al. 1980). Estimated density of J. ashei in central Texas
ranges from approximately 700 trees ha 1 to 1500 trees ha 1 (Van Auken
et al. 1979; Smeins 1990).

Evidence suggests that J . ashei, as well as some other species of

THE TEXAS JOURNAL OF SCIENCE- VOL. 56, NO. 1, 2004

Juniperus, have increased in density since European settlement by
encroachment into adjacent grasslands (Buechner 1944; Smeins 1980;
Fuhlendorf et al. 1996; Van Auken 2000). Historically, 7. ashei was
apparently restricted to canyons, rocky outcrops or areas with shallow
soils, which were protected from grassland fires (Ellis & Schuster 1968).
The most widely cited explanation for woody plant encroachment
attributes the shifts in community types to a concomitant reduction in
fire frequency and decreased competition from grasses, both of which
are promoted by heavy grazing by domestic ungulates (Neilson 1986;
Archer et al. 1988; Schlesinger et al. 1990; Bashre 1991; Van Auken
2000).

There are many reports of allelopathic effects of litter or litter extracts
on various understory species, including woody plant seedlings (Rice
1984). Suppression of understory vegetation by 7. osteosperma is
commonly reported in New Mexico and Arizona (Arnold et al. 1964)
and 7. virginiana and 7. pinchott may reduce herbaceous cover and
diversity (Arnold et al. 1964; Engle et al. 1987; Armentrout & Pieper
1988). Juniperus monosperma litter seems to have a negative effect on
the growth of Bouteloua gracilis (blue grama) (Jameson 1966; Jameson
1970b). In addition, reduction of herbaceous vegetation has been
reported below Juniperus canopies even after canopy removal (Bonnett
1960; Jameson 1966; Jameson 1970b; Carson 1990; Barnes & Archer
1996). However, the cause of the apparent allelopathic effects is
unclear.

Juniperus ashei has been observed with a zone of reduced herbaceous
cover and diversity beneath the crown near the stem (Blomquist 1990;
Fuhlendorf 1992). In closed-canopy stands, J. ashei like other
Juniperus sp. can exclude most herbaceous vegetation (Buechner 1944;
Johnsen 1962; Burkhart & Tisdale 1969; Yager & Smiens 1999). How¬
ever, there are some places below the canopy that Car ex pianos tacky s
(cedar sedge) has high cover (Wayne 2000; Wayne & Van Auken 2002).
Juniperus ashei tree litter was demonstrated to have negative effects on
seedling recruitment and germination of some herbaceous species
including grasses, but negative effects were reduced or absent on a
woody plant seedling ( Sophora secundiflora ) by Yager & Smeins (1999).
In addition, litter apparently reduced the density of most woody and
herbaceous species even after adult 7. ashei canopies were completely
removed (Yager & Smeins 1999). However, 7. ashei seedlings have
been observed to rapidly establish following the removal of the adult

McKINLEY & VAN AUKEN

canopy (Weniger 1984; Owens 1995).

Juniperus ashei seedlings below the adult canopy in woodlands have
a lower mortality and lower growth rates than seedlings near the canopy
edge adjacent to grasslands or gaps (Jackson & Van Auken 1997).
Juniperus ashei seedlings in these woodlands decreased exponentially
through time with 1-18% surviving eight years, depending on the
cohort. Gradients of light levels, soil moisture, organic content and
surface temperatures occur from under the adult J. ashei canopy into the
adjacent grasslands or gaps (Wayne 2000; Wayne & Van Auken 2002).
It seems clear that adult J. ashei trees have a direct or indirect influence
on the growth and survival of J. ashei seedlings. Part of this influence
may be caused by the presence of J. ashei tree litter.

Tree litter has been shown to have a mixed influence on the growth
and development of canopy tree seedlings. Negative influences may
include shading, crushing, allelopathy, limiting water absorption and
isolation of the seedling roots from the mineral soil (Johnsen 1962;
Bergelson 1990; Bosy & Reader 1995; Milton 1995; Yager & Smiens
1999). There are also some positive influences that have been associated
with tree litter, including reduction in competition from herbaceous
species, protection from desiccation, increased soil aeration and nutrient
release from litter decomposition (Fowler 1986; Facelli & Pickett 1991;
Facelli 1994; Yager & Smiens 1999). The purpose of this study was to
examine the potential effects of J. ashei tree litter on the growth and
survival of J. ashei seedlings.

Materials and Methods

This study was conducted for five months from 15 June 2001 to 15
November 2001 at the University of Texas at San Antonio in a forced
air, temperature controlled (21-29°C) fiberglass greenhouse. Light
levels for photosynthetically active radiation (PAR, X = 400 to 700 nm)
were * 400 /xmole m' 2 s'1 inside the greenhouse and under 50% shade
cloth on a cloudless day at solar noon on 7 September 2001 (22% of
outdoor ambient light), which approximated light levels under intact J .
ashei canopies. Light levels were measured with a LI-COR® LI- 1 90S A
integrating quantum sensor and recorded using a LI-COR® LI- 1000 Data
Logger using a 60 s average (5 s intervals).

Juniperus ashei tree litter was collected in Eisenhower Park
(29°37’19"N, 98°34’26"W, 322 m height above ellipsoid, in northern

THE TEXAS JOURNAL OF SCIENCE— VOL. 56, NO. 1, 2004

Bexar County) on 1 May 2001 from under ten J. ashei trees. At each
J. ashei tree, five 0.1m2 sites with tree litter present were arbitrarily
chosen. The tree litter (O-horizon) was comprised mainly of debris in
various stages of decomposition (fresh to highly decomposed) from the
adult J. ashei trees, which included leaves, cones, bark, small branches
and seeds. Five approximately equal samples from under each sampled
tree were collected to a maximum depth of approximately 10 cm with
a hand trowel and placed in a large plastic trash bag. The cumulative
sample from all ten J. ashei trees was mixed thoroughly by hand and
spread out on the cement greenhouse floor and air-dried for 14 d.
Schultz® Horticultural Vermiculite was used as a control to simulate the
physical, but not chemical properties of J . ashei litter. The vermiculite
was washed thoroughly with approximately 15 liters of deionized water
in 25 liters containers. The excess water was then poured off and the
remaining vermiculite was spread out and air-dried on the greenhouse
floor in a comparable fashion as the J. ashei litter.

Recently emerged J. ashei seedlings (only cotyledons present) were
transplanted from Eisenhower Park, into 15 by 15 cm plastic pots lined
with Ziploc® bags to prevent water and nutrient loss ( n = 72). Each pot
was filled with 800 g of sieved (4 mm mesh), air-dried, low nutrient,
non-fertilized, clayey over sandy or sandy skeletal, carbonatic, thermic
Typic Calciustoll (United States Department of Agriculture, 2000) in the
Patrick association, obtained in northern Bexar County. Fertilizer was
not added because the growth of J. ashei seedlings did not appear to be
limited (having substantial growth) in prior experiments, which used the
same soil and approximately the same mass. On 15 May 2001 pots
were randomly assigned treatments that consisted of adding different
levels of J. ashei tree litter or vermiculite. Treatments of 0, 50, 100,
150, 200 and 250 g (n = 6 for each level) of either washed, air dried
vermiculite or air dried J. ashei tree litter were placed on top of the
mineral soil with care given to prevent the burial of the J. ashei
seedlings. All pots were initially watered with 300 mL of deionized
water after transplantation. Seedling treatments were initially random¬
ized on greenhouse tables for treatment and replicate, and to minimize
edge effects were rearranged randomly every 2 wk. The pots were
watered as needed with 50-150 mL of deionized water (every 4-8 days).
Seedlings were allowed 30 d from the initial transplantation to recover
from any transplant shock. During the transplant recovery period (15
May - 15 June) 13 seedlings died, and were not considered in the study.
Thus, total n = 59 and sample size per treatment were unequal.

MCKINLEY & VAN AUKEN

Basal diameter, height and number of branches were measured for
each J. ashei seedling at the beginning of the experiment (15 June 2001)
and at the termination of the experiment (1 1 November 2001). A 1 mm
dot of nail polish was used to mark all J. ashei seedlings on the main
stem 3 cm from the top of the mineral soil. All basal diameter measure¬
ments were made immediately above this mark using a digital caliper
(Mitutoyo®, model CD-6”P). Each basal diameter measurement,
measured in millimeters, was a mean of six measurements; the first three
were taken from the north to south facing direction of the seedling and
the last three at the east and west facing direction of the J. ashei
seedling. Juniperus ashei seedling height, measured in centimeters, was
measured from the nail polish mark to the top of the leaves on the
uppermost living branch of the seedling. The number of branches for
each J. ashei seedling was determined by counting all living branches
greater than 2 mm in length. When branches or entire seedlings were
presumed to have died (green tissue was no longer visible) response
variables were not measured, and a zero was recorded for its measure¬
ment.

Absolute differences in growth (final measurement minus initial
measurement) for basal diameter, height and number of branches were
analyzed with a two-way AN OVA with interaction to determine signifi¬
cant differences between litter types (2 levels) and amounts (6 levels).
Also, numbers of seedling mortalities were analyzed between the litter
treatment types and amounts with chi- squared analysis. Expected values
for the chi-squared analysis were adjusted to account for unequal initial
sample size by multyplying cumulative mean percent mortality by the
initial sample size.

Results

The overall models for the two-way AN OVA ’s of the absolute differ¬
ences in growth of the three response variables were not significant
(basal diameter F = 1.41, P — 0.20, basal diameter F = 1.43, P =
0. 19, basal diameter F = 1.00, P = 0.46), which indicated that there
were no significant differences between litter types and amounts, or the
two-way interaction.

Generally, seedlings in the vermiculite treatment had greater absolute
differences in growth for height, branches, and basal diameter than their
J. ashei litter counterparts (24% for height and 3% for number of
seedling branches and 13% for basal diameter) , but again none of these

THE TEXAS JOURNAL OF SCIENCE- VOL. 56, NO. 1, 2004

Table 1. Sample size, absolute final mean (+ SD) growth difference (final minus initial
measurements), in the J. ashei litter and vermiculite treatments. Although there is a
decrease in the response variables with increased litter inputs, there are no significant
differences between any of the response variables with litter types or amounts (two-way
AN OVA ’s). Some measures of variance (SD) are not reported (na), due to small or
missing samples.

Sample ( n ) Basal diameter (mm) Height (cm) # of Branches

Litter J/V J. ashei Vermicu- J. ashei Vermicu- J. ashei Vermicu-
amount litter litter lite litter lite litter lite

6/4

0.00

0.14

0.07

0.05

2.68

1.81

4.61

1.29

3.0

2.6

2.0

6/6

0.14

0.15

0.35

0.29

2.40

0.58

2.78

1.58

4.6

2.1

4.0

3.6

100

6/5

0.20

0.25

0.21

0.04

2.83

2.99

1.00

0.85

4.5

6.4

3.5

0.7

150

4/5

0.11

0.24

0.03

1.73

0.59

3.20

3.0

9.0

200

4/5

0.05

0.00

1.65

0.78

0.00

1.0

1.4

0.0

250

5/3

0.00

0.0

differences were significant (Table 1). Fifty g of J . ashei litter and
vermiculite had the greatest increase in mean absolute differences for
basal diameter (86%) and number of branches (42%), alternately mean
absolute differences for height decreased (41% less) compared to no
litter and no vermiculite treatments. Mean absolute differences generally
decreased with increased amounts of both litter types over 50 g, until
100% mortality occurred in the 200 g and 250 g of vermiculite and in
250 g of J. ashei litter. Standard deviations were large, being equal to
the treatment mean in many cases (Table 1).

Seedling mortalities were analyzed between the litter treatment types
and amounts to determine if a particular treatment or treatments induced
greater mortality. There were no significant differences in mortality
between vermiculite (19) and 7. ashei (13) litter ( X 2 = 2.01, P = 0. 16,
df 1) (Table 2). Although mortality in both treatments increased with
increased amounts of J. ashei litter or vermiculite (ranging from 25-
100%), there were also no significant differences in mortality with
respect to litter amounts of both treatments combined ( X 2 = 6.46, P =
0.26, df 5).

Discussion

An allelopathic effect claimed for litter of some species of Juniperus
(Jameson 1970a; Jameson 1970b; Whittaker & Feeney 1971; Everett et
al. 1983; Rice 1984) and for the litter of many other species (Rice 1984)
was not demonstrated in the present study. Allelopathic substances, if
present, may be transitory due to rapid decomposition of possible growth

McKINLEY & VAN AUKEN

Table 2. Seedling mortalities in the J. ashei litter and vermiculite treatments, including
number of mortalities for both types and amount of litter. The initial sample size n is
given in parenthesis. There were no significant differences in mortality between the litter
types (X2 = 2.01, P = 0.16, df 1). There were also no significant differences in
mortality with respect to litter amounts of both treatments combined (X2 = 6.46, P =
0.26, df 5).

Litter Amount
(g)

% Mortality

Tree Litter

Vermiculite

Mean

0(10)

33% (6)

50% (4)

40%

50 (12)

17% (6)

33% (6)

25%

100 (11)

33% (6)

60% (5)

45%

150 (9)

25% (4)

80% (5)

55%

200 (9)

50% (4)

100% (5)

78%

250 (8)

100% (5)

100% (3)

100%

Mean

42% (n ==31)

68% (n = 28)

54% (n= 59)

inhibitors in the litter (Jameson 1970a) or leaching from the system
(Rice 1984). The effects observed in the present study appear to be
caused by physical effects independent of the litter type used. The
effects of these organic (J. ashei litter) and inorganic (vermiculite)
substances in terms of absolute differences in growth and mortalities
appear not only to be statistically homologous between treatment type,
but also the trends appear to be similar across treatment amounts. These
patterns strongly suggest that an allelopathic component in the J. ashei
litter was not present and consequently had little or no influence on the
growth of the J . ashei seedlings.

Differences in mortality between the J. ashei tree litter and vermicu¬
lite (control) treatments overall (Table 2) indicate that the seedling
mortality was lower in the J. ashei litter treatment (42%) compared to
the vermiculite treatment (68%), but very high mortality (100%) was
found in the J . ashei litter and also in the vermiculite. An organic
component cannot be ruled out as positively influencing J. ashei seedling
mortality, because of observed decreases in seedling mortality in the
lower J. ashei litter treatments. However, the same trend was found in
the vermiculite treatment.

Some positive effects of litter in field situations have been cited,
which are conservation of water during dry conditions (Fowler 1986)
and adding nutrients to the soil after litter decomposition (Facelli &

THE TEXAS JOURNAL OF SCIENCE- VOL. 56, NO. 1, 2004

Pickett 1991). Nutrients released from the J. ashei litter or moisture
loss prevention properties of the litter are not plausible explanations for
the observed changes in growth and mortality in the present study.
Vermiculite is thought to have provided little or no nutrients to the soil
during the experimental period. Consequently, the positive effects on
seedling growth seen by both litter types at low addition levels were not
likely a nutrient effect. The hydrophobic effects that litter may have
(Gifford 1970; Yager & Smiens 1999), which could limit, or conversely
improve water availability for the seedlings in field settings were not
tested in the current study, because the study attempted to reduce
unwanted variability by keeping the soil moist at all times. Further¬
more, the observed effects cannot be attributed to prevention of the
seedling roots reaching the mineral soil since the seedlings in this study
were initially planted in mineral soil.

The small increase in the mean absolute growth differences and
decreased mortality (25% compared to the mean of 54% for all seedling
treatments) of the seedlings in the 50 g litter treatments (cumulative for
J. ashei and vermiculite litter) in the present study may have been
caused by soil aeration. Aeration by plant litter has been shown to
occur, and it is important in rooting depth, root respiration and even
nitrogen fixation in some plants (Khan et al. 2000). Greater aeration
could have been caused inadvertently in the present study by small
amounts of mixing of the upper soil layers in both litter types during the
initial setup.

Indirect influence of the litter on other organisms closely associated
with the J. ashei seedlings in the field should also be considered.
Juniperus ashei tree litter or vermiculite may facilitate a favorable
microenvironment (temperature and moisture), benefiting soil animals,
fungi or microorganisms (Sylvia et al. 1998). The favorable micro¬
climate may facilitate nitrogen mineralization, increasing inorganic
nitrogen availability, which is a primary limiting nutrient in most North
American terrestrial ecosystems. Also, existing relationships that J.
ashei seedlings may have with various organisms may also depend on
the presence of J. ashei litter for a labile carbon source, ultimately
enhancing nitrogen availability.

The effects of litter may be difficult to demonstrate in field settings,
because the presence of litter may alter resource availability so that litter
suppression and resource competition are interlinked, and therefore

MCKINLEY & VAN AUKEN

confounding (Foster & Gross 1997; Foster & Gross 1998). Jackson &
Van Auken (1997) found that seedling mortality was lowest under intact
canopies, which have substantial amounts of J. ashei litter. Findings
from this current study corroborate this previous observation, that J.
ashei litter apparently does not interfere with J . ashei seedling growth
and potentially may even enhance growth and lower mortality for
seedlings growing in shallow O-horizons. In a field setting, reduction
of herbaceous vegetation including grass species in J . ashei woodlands
might be important for the initial establishment of the J. ashei seedlings,
possibly until both the roots of the J. ashei seedlings are beyond depth
of root competition and aboveground competition for light is reduced.
A possible mechanism of intraspecific seedling facilitation by the adult
J. ashei trees and specifically J. ashei litter may be the reduction in
competition from herbaceous and other woody species, in addition to an
improvement in seedling growth and mortality caused by the physical
presence of underlying litter. However, large amounts of J. ashei litter
may reduce the growth and survival of the J. ashei seedlings, as well as
competing species, forfeiting any potential advantage the presence of the
litter may provide for J. ashei seedlings. Juniperus ashei litter may play
an important part in J. ashei seedling establishment, ultimately affecting
the replacement and population dynamics of this species, but this role
appears difficult to detect.

Acknowledgments

The College of Science and Department of Biology at the University
of Texas at San Antonio provided support for this project. The support
of W. and L. Collenback through a generous scholarship is most
appreciated. I would like to thank E. Lautzenheiser who represented the
City of San Antonio Parks Department, for allowing me to remove
seedlings at Eisenhower Park. Also, I would like to thank Marisela R.
McKinley, who helped me find and procure seedlings for this study.

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DM at: Duncanmc40@hotmail.com

TEXAS J. SCI. 56(1): 15-34

FEBRUARY, 2004

THE VASCULAR FLORA OF

THE PALO ALTO NATIONAL BATTLEFIELD HISTORIC SITE,
CAMERON COUNTY, TEXAS

Robert I. Lonard*, Alfred T. Richardson and
N. L. Richard

Department of Biology, University of Texas-Pan American
Edinburg, Texas 78541-2999 * and
Department of Biology, University of Texas at Brownsville
Brownsville, Texas 78520

Abstract.— A checklist is provided of the vascular plant taxa of the 1,376 ha Palo Alto
Battlefield National Historic Site (PABNHS) in Cameron County of south Texas. PABNHS
consists of four plant communities: resacas and tanks, salt flats, brush-grasslands and coastal
marshes. Vascular plants of disturbed sites are noted. Two hundred forty-three taxa in 66
families are documented and their community affiliations are given. Three families, Poaceae,
Asteraceae and Fabaceae contain 37.5% of the species richness at PABNHS.

The southernmost extension of prairie in the United States is located
in the Gulf Prairies and Marshes vegetation area of Texas (Schuster &
Hatch 1990). Saline sites in the prairie in southern Texas that are
flooded intermittently are usually dominated by Spartina spartinae (gulf
cordgrass), often to the exclusion of other species (Oefinger & Scifres
1977; Scifres et al. 1980; Smiens et al. 1991). Kuchler (1964)
combined upland Andropogon/ Schizachyrium and/or Bothriochloa
prairies with S. spartinae marshes and referred to the entity as a
Southern Cordgrass Prairie, and Diamond et al. (1987) referred to this
community as a Gulf Cordgrass Series. Turner (1959), the only investi¬
gator using quantitative methods, mapped most of south Texas in the
Tamaulipan ecoregion (MacRoberts & MacRoberts 2003).

Johnston (1955; 1963) stated that the poorly drained flats near the
coast in Cameron County support a salt prairie. He reported that the
area is dominated by halophytic subshrubs including Bat is maritima ,
Salicomia virginica, Suaeda sp., Borrichia frutescens and the mat¬
forming grass, Monanthochloe littoralis. Low-lying saline, sometimes
water-logged clays at elevations from 0 m to 3 m above sea level are
referred to as "Borrichia flats" (Johnston 1955; 1963). Lonard et al.
(1991) partitioned the natural vegetation of the lower Rio Grande Valley
into four major habitats (1) Rio Grande floodplain, (2) coastal prairies
and marshes, (3) barrier islands and (4) brush-grasslands, and they
provided brief descriptions of these habitats.

THE TEXAS JOURNAL OF SCIENCE— VOL. 56, NO. 1, 2004

The U.S. National Park Service proposes to restore the battlefield
landscape at the Palo Alto National Battlefield National Historic Site
(PANBHS) to the putative conditions at the time of the first battle of the
Mexican- American War (1846-1848). U. S. Grant noted in his war
diary that the grass ( S . spartinae) that dominated the wet battlefield . . .
"was tall, reaching the shoulders of the men, very stiff, and each stock
pointed at the tip, and hard, almost as sharp as a darning needle"
(Sanchez 1985). The restoration will include the highly disturbed core
battlefield site in the coastal marsh formerly dominated by gulf cordgrass
and the adjacent resaca (remnant shallow, abandoned river channel of
the historic floodplain of the lower Rio Grande) that provided water for
the combatants.

Little is known about the extant vascular plant species richness of this
National Historic Site. Only one unpublished checklist of vascular
plants is available (Richard & Richardson 1993) for the site. Thus there
has been no comprehensive study of the flora of PANBHS. The purpose
of this paper is to identify the vascular flora of this segment of the Rio
Grande Delta.

Study Site

A broad delta has been formed by the Rio Grande on the Texas
mainland where the river approaches the Gulf of Mexico. The delta
fronts the coastline from 25° 30’ to 26° 30’ N latitude between Port
Mansfield in Willacy County and the mouth of the Rio Grande in
Cameron County. At least three major Holocene lobes were formed by
the Rio Grande fluvial -deltaic system (Brown et al. 1980). The study
site, characterized by numerous resacas, is located in the Del Tigre
intermediate sub-delta where the river shifted into Mexico. The north¬
western extension of the delta is 67 km upstream from the Gulf of
Mexico and includes all of Cameron County (Clover 1937; Brown et al.
1980; Judd & Lonard 2002).

PANBHS about 16.1 km north of the Rio Grande is located at the
intersection of two roads, F.M. 511 and F.M. 1487, in Cameron
County, Texas. The 1,376 ha National Park Unit is in a broad,
undeveloped prairie interspersed with stands of mixed brush and several
lengthy resacas. The area is in the Matamoros district of the
Tamaulipan Biotic Province (Blair 1950).

All soils at PANBHS are saline clays or clay loams (Table 1)
(Williams et al. 1977). The highly saline Lomalta Clay is the predomi¬
nant soil series. It includes the substrate of the core battlefield site and

LONARD, RICHARDSON & RICHARD

Table 1 . Soil series and vegetation zones at Palo Alto National Battlefield Historic Site. RT
= resacas and tanks, SF = salt flats, CM = coastal marshes and BG = brush-grasslands.

Soil Series

Percent of Area

Vegetation Zones

Lomalta clay

62.6

RT, SF, CM

Chargo silty clay

12.9

Laredo silty clay loam, saline

8.4

RT margins, SF, CM

Laredo silty clay loam

6.0

Sejita silty clay loam

5.0

CM, SF

Latina sandy clay

2.9

SF, CM

Benito clay

2.2

CM, SF

resaca systems. Vegetation zones that occur here are coastal marshes
(S. spartinae community), salt flats and resacas and tanks. The less
saline Chargo Silty Clay and Laredo Silty Clay Loam Series (18.9%) of
the area occur at elevations greater than 4.6 m above sea level and
support brush-grassland vegetation (Table 1). The topography is flat,
and the elevation is 2.96 m to 6.37 m above sea level. The water table
typically ranges from 45 to 91 cm below the soil surface (Williams et al.
1977).

The climate of the area is semi-arid (Thornth waite 1948) with an
annual precipitation of about 66 cm (Lonard et al. 1991). Rainfall peaks
are in September and October. The mean frost free period is 330 days,
and frequently an entire winter will pass without freezing temperatures
(Lonard et al. 1991).

Although the site retains some of its original integrity, most of
PANBHS has been disturbed. Resaca channels have been excavated or
blocked to form small tanks. Grazing, farming, road building and
excavation of drainage canals have altered landscape features. Aban¬
doned cultivated fields, established in the 1940’s, occupy the core
battlefield area, and secondary succession has not resulted in the return
of a S. spartinae community.

Methods

Data reported here are based primarily on collections made by
Richardson and Richard in 1992 and 1993 and by Richardson in 1991.

THE TEXAS JOURNAL OF SCIENCE- VOL. 56, NO. 1, 2004

Table 2. Summary of the vascular flora of Palo Alto Battlefield National Historic Site,
Cameron County, Texas.

Polypodiopsida

Magnoliopsida

Liliopsida

Total

Families

Genera

148

188

Species

182

243

Native species

170

223

Introduced species

Lonard conducted monthly surveys between June and November 2001
and from December 2002 to June 2003. Vouchers were deposited in the
University of Texas-Pan American Herbarium (PAUH). Nomenclature
including common names follows Jones & Wipff (2003). Abbreviations
are used to refer to vegetation zones or sites recognized in Lonard et al .
(1991). A category, disturbed sites, has been added to include areas
altered by farming, grazing, or road construction. Abbreviations and
vegetation zones and sites are:

RT - Resacas and tanks

SF - Salt flats

CM - Coastal marshes

BG - Brush-grasslands

DS - Disturbed sites

I - Introduced

Results and Discussion

This study reports the presence of 243 species of vascular plants
representing 188 genera and 66 families from PANBHS (Table 2). The
three most common families are Poaceae (16.5%), Asteraceae (15.2%)
and Fabaceae (5.8%). Thirty families are represented by a single
species, and 20 species have been introduced.

LONARD, RICHARDSON & RICHARD

CHECKLIST OF THE VASCULAR FLORA OF THE
PALO ALTO NATIONAL HISTORIC SITE,
CAMERON COUNTY, TEXAS

POLYPODIOPSIDA (FERNS)

MARSILEACEAE

Marsilea macropoda (G. Engel mann ex A. Braun) A. Gray.
Water-clover, (RT).

MAGNOLIOPSIDA (DICOTS)

ACANTHACEAE

Dyschoriste crenulata C. Kobuski. Crenate-leaf snake-herb, (BG).
Elytraria bromoides A. Oersted. Wheat-spike scaly-stem, (BG).
Justicia pilosella (C. Nees von Esenbeck) R. Hilsenbeck.
Tube- tongue, (BG).

Ruellia nudiflora (G. Engelmann ex A. Gray) I. Urban var. runyonii
(B. Tharp & F. Barkley) B.L. Turner. Runyon’s violet wild-petunia,
(BG).

Stenandrium dulce (A. Cavanilles) C. Nees von Esenbeck. Sweet
shaggy-tuft, (BG).

ACHATOCARPACEAE

Phaulothamnus spinescens A. Gray. Snake-eyes, (BG).
AIZOACEAE

Sesuvium verrucosum C. Rafinesque-Schmaltz. Winged sea-purslane,
(RT, DS, SF).

Trianthema portulacastrum C. Linnaeus. Desert horse purslane,
(DS).

AMARANTHACEAE

Altemanthera paronychioides A. de Saint-Hilaire. Smooth joy weed,
(RT).

Amaranthus blitoides S. Watson. Prostrate pigweed, (DS, I).
Celosia nitida M. H. Vahl. West Indian cock’s-comb, albahaca,
(BG).

THE TEXAS JOURNAL OF SCIENCE- VOL. 56, NO. 1, 2004

APIACEAE

Cyclospermum leptophyllum (C. Persoon) T. A. Sprague ex N. Britton
& Percy Wilson. Slim-lobe celery, (DS, I).

Eryngium nasturtiifolium A.L. de Jussieu ex F. Delaroche. Hierba
del sapo, (RT, DS).

ASCLEPIADACEAE

Cynanchyum barbigerum (G. Scheele) L. Shinners. Swallow- wort,
(BG, DS).

ASTERACEAE (Compositae)

Acourtia runcinata (M. Lagasca y Segura ex D. Don) B.L. Turner.
Stemless desert peonia, (BG).

Aphanostephus ramosissimus A. P. de Candolle. Plains lazy-daisy,
(DS).

Ambrosia psilostachya A. P. de Candolle. Western ragweed, (DS).
Baccharis neglecta N. Britton. Roosevelt weed, (DS).

Bidens laevis (C. Linnaeus) N. Britton, E. Sterns & J. Poggenbery.
Smooth beggar-ticks, (RT).

Borrichia frutescens (C. Linnaeus) A.P. de Candolle. Sea-ox-eye
daisy, (RT, SF, CM, DS).

Calyptocarpus vialis C. Lessing. Straggler daisy, (DS).
Chromolaena odorata (C. Linnaeus) R. King & B. Robinson.
Crucita, (BG, DS).

Cirsium texanum S. Buckley. Southern thistle, (DS).

Clappia suaedifolia A. Gray, Fleshy-leaf clappia, (SF, DS).
Coreopsis tinctoria T. Nuttall. Golden wave, (RT, DS).

Dyssodia pentachaeta (A.P. de Candolle) B. Robinson. Parralena,
(BG, DS).

Dyssodia tenuiloba (A.P. de Candolle) B. Robinson var. treculii
(A. Gray) J. Strother. Bristleleaf dyssodia, (BG, DS).

Eclipta prostrata (C. Linnaeus) C. Linnaeus. Yerba de tago,
(RT).

Erigeron tenellus A.P. de Candolle. Fleabane, (DS).

Evax vema C. Rafinesque-Schmaltz. Spring evax, (DS).
Fleishmannia incamata (T. Walter) R. King & H. Robinson.
Flesh-pink fleishmannia, (BG, DS).

Florestina tripteris A. P. de Candolle. Three-lobed florestina, (DS).
Gamochaeta falcata (J. de Lamarck) A. Cabrera. Sickle cudweed,
(DS, I).

Gamochaeta pensilvanica (C. von Wildenow) A. Cabrera. Purple

LONARD, RICHARDSON & RICHARD

cudweed, (DS).

Gutierrezia texana (A. P. de Candolle) J. Torrey & A. Gray. Texas
snakeweed, (DS).

Helenium microcephalum A.P. de Candolle var. ooclinum (A. Gray)
M. Bierner. Sneeze- weed, (RT).

Helianthus annuus C. Linnaeus. Sunflower, (DS).

Isocoma drummondii (J. Torrey & A. Gray) Greene. Drummond’s
jimmy weed, (BG, DS).

Machaeranthera phyllocephala (A. P. de Candolle) L. Shinners.
Camphor tansy-aster, (SF, DS).

Packera tampicana (A. P. de Candolle) C. Jeffrey. Tampico
butter weed, (RT, DS).

Parthenium hysterophorus C. Linnaeus. Ragweed parthenium, false
ragweed, (DS).

Pluchea purpurascens (O. Swartz) A. P. de Candolle. Purple
marsh- fleabane, (RT).

Senecio ampullaceus W. Hooker. Groundsel, (BG, Texas endemic).
Simsia calva (G. Engelmann & A. Gray) A. Gray. Bush sunflower,
(BG).

Sonchus asper (C. Linnaeus) J. Hill. Rough sow thistle, (DS, I).
Sonchus oleraceus C. Linnaeus. Common sow thistle, (DS, I).
Symphyotrichum divaricatum (T. Nuttall) G. Nesom. Wireweed,
salt-marsh aster, (DS, RT).

Trichocoronis wrightii (J. Torrey & A. Gray) A. Gray. Wright’s
bugheal, (RT, CM).

Verbesina encelioides (A. Cavanilles) G. Bentham & J. Hooker ex A.
Gray. Cowpen daisy, (DS).

Verbesina microptera A.P. de Candolle. Capitana crownbeard, (BG,
DS).

Wedelia texana (A. Gray) B. L. Turner. Texas wedelia, (BG).
BATACEAE

Batis maritima C. Linnaeus. Maritime saltwort, vidrillos, (RT, SF,
CM).

BORAGINACEAE

Heliotropium angiospermum J. Murray. Taper-leaf heliotrope, (DS,
RT).

Heliotropium curas savicum C. Linnaeus. Seaside heliotrope, (RT,
SF, CM, DS).

THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 1, 2004

BRASSICACEAE

Lepidium austrinum J. K. Small. Southern pepperwort, (DS).
Lepidium lasiocarpum T. Nuttall ex J. Torrey & A. Gray var.
wrightii (A. Gray) C. Hitchcock. Wright’s woolly-fruit pepperwort,
(DS).

Lesquerella argyraea (A. Gray) S. Watson. Narrow-leaf bladderpod,
(DS).

Lesquerella lasiocarpa (W. Hooker ex A. Gray) S. Watson var.
berlandieri (A. Gray) E. Payson. Berlandier’s woolly-pod
bladderpod, (DS).

Sisymbrium irio C. Linnaeus. London rocket, (DS, I).
CACTACEAE

Acanthocereus tetragonus (C. Linnaeus) E. Hummel. Barb- wire
cereus, (BG).

Cylindroopuntia leptocaulis (A.P. de Candolle) K. Kunth. Tasajillo,
desert Christmas cactus, (BG, DS).

Echinocactus texensis C. Hopffer. Devil’s head, (BG).
Echinocereus pentalophus (A. P. de Candolle) C. Lemaire.
Lady-finger hedge-hog cactus, (BG).

Mammillaria heyderi F. Miihlenpfordt. Heyder’s pinchusion cactus,
(BG).

Opuntia engelmannii J. Salm-Reifferscheid-Dyck. Engelmann’s
prickly pear, (BG, DS).

Telocactus setispinus (G. Engelmann) E. Anderson. Miniature barrel
cactus, (BG).

CAMPANULACEAE

Lobelia berlandieri A. L. de Candolle. Lobelia, (DS).
CAPPARACEAE

Koeberlinia spinosa J. Zuccarini. Allthorn, crucifixion- thorn, (BG).
CELASTRACEAE

Maytenus phyllanthoides G. Bentham. Mangle-dulce, (BG, SF, DS).
Schaefferia cuneifolia A. Gray. Desert yaupon, (BG).

CHENOPODIACEAE

Atriplex matamorensis A. Nelson. Matamoros saltbush, (SF, DS).
Atriplex pentandra (N. von Jacquin) P. Standley. Quelite saltbush,
(SF, DS).

LONARD, RICHARDSON & RICHARD

Chenopodium berlandieri C. Moquin-Tandon. Goosefoot, (DS).
Chenopodium murale C. Linnaeus. Nettle-leaf goosefoot, (DS, 1).
Salicomia virginica C. Linnaeus. Perennial saltwort, (SF).

Suaeda linearis (S. Elliott) C. Moquin-Tandon. Annual seepweed,
(SF, DS).

Suaeda tampicensis (P. Standley) P. Standley. Tampico seepweed,
(SF, DS).

CLUSIACEAE

Hypericum pauciflorum K. Kunth. Few-flowered St. John’s wort,
(BG, DS).

CONVOLVULACEAE

Dichondra micrantha I. Urban. Small-flowered pony foot, (BG, DS).
Evolvulus alsinoides (C. Linnaeus) C. Linnaeus var. angustifolius J.
Torrey. Ojo de vfbora, (BG, DS).

Evolvulus sericeus O. Swartz. Silky dwarf morning glory, (DS).
CRASSULACEAE

Kalanchoe delagoensis C. Ecklon & C. Zeyher. Kalanchoe, (DS, I).
Lenophyllum texanum (J. G. Smith) J. Rose. Texas stonecrop, (BG).

CUCURBITACEAE

Ibervillea lindheimeri (A. Gray) E. Greene. Lindheimer’s
globeberry, (BG, DS).

Melothria pendula C. Linnaeus. Drooping melonette, (DS).
EUPHORBIACEAE

Chamaesyce serpens (K. Kunth) J.K. Small. Matted sand-mat, (DS).
Croton capitatus A. Michaux var. lindheimeri (G. Engelmann & A.
Gray) J. Muller of Aargau. Lindheimer’s hogwort croton, (DS).
Croton leucophyllus J. Muller of Aargau. Croton, (DS).

Ditaxis humilus (G. Engelmann & A. Gray) F. Pax. Low-growing
silverbush, (DS).

Jatropha cathartica M. Teran & J. Berlandier. Geranium- flowered
jatropha, (BG).

Jatropha dioica M. Sesse y Lacasta ex V. de Cervantes.
Leather-stem, (BG).

Phyllanthus polygonoides T. Nuttall ex K. Sprengel. Knot weed leaf
flower, (DS).

THE TEXAS JOURNAL OF SCIENCE— VOL. 56, NO. 1, 2004

FABACEAE (Leguminosae)

Acacia famesiana (C. Linnaeus) C. von Willdenow. Huisache,
(CM, RT, DS).

Chloroleucon ebano (J. Berlandier) L. Rico. Texas ebany, (BG).
Dalea pogonothera A. Gray var. walkerae (B. Tharp & T. Barkley)
B.L. Turner. Bearded dalea, (DS).

Dalea scandens (P. Miller) R. Clausen var. paucifolia (J. Coulter) R.
Barneby. Low dalea, (BG).

Desmanthus virgatus (C. Linnaeus) C. von Willdenow var. depressus
(F. von Humboldt & A. Bonpland) ex C. von Willdenow) B. L.
Turner. Bundled ower, (DS).

Leucaena pulverulenta (D. von Schlechtendal) G. Bentham.
Tepeguaje, (BG).

Melilotus albas F. Medikus. White sweetclover, (DS, I).

Mimosa asperata C. Linnaeus. Black mimosa, (RT).

Mimosa strigillosa J. Torrey & A. Gray. Pink sensitivebrier, (DS).
Parkinsonia aculeata C. Linnaeus. Retama, (BG, RT, CM, DS).
Prosopis glandulosa J. Torrey. Mesquite, (BG, CM, RT, DS).
Prosopis reptans G. Bentham var. cinerascens (A. Gray) A.
Burkhart. Creeping mesquite, tornillo, (RT, SF, CM, DS).
Sesbania drummondii (P. Rydberg) V. Cory. Drummond’s
rattlebush, poison bean, (RT).

Sesbania herbacea (P. Miller) R. McVaugh. Large-fruited rattlebush,
(RT).

GENTIANACEAE

Eustoma exaltatum (C. Linnaeus) A. Salisbury ex G. Don. Tall
prairie gentian, bluebell gentian, (RT, DS).

HYDROPHYLLACEAE

Narna hispidum A. Gray. Rough nama, (DS).

Nama jamaicense C. Linnaeus. Jamaican nama, (DS).

LAMIACEAE

Micromeria brownei (O. Swartz) G. Bentham var. pilosiuscula A.
Gray. Browne’s savory, (RT).

Salvia coccinea P. Buc’hoz ex A. Etlinger. Scarlet sage, (BG, RT).
Teucrium cubense N. von Jacquin. Germander, (BG, DS).

LYTHRACEAE

Ly thrum alatum F. Pursh var. lanceolatum (S. Elliott) J. Torrey & A.

LONARD, RICHARDSON & RICHARD

Gray ex J. Rothrock. Lance-leaf loosestrife, (RT, DS).

Ly thrum califomicum J. Torrey & A. Gray. California loosestrife,
(RT, DS).

MALVACEAE

Abutilon trisulcatum (N. von Jacquin) I. Urban. Anglestem abutilon,
(BG, DS).

Anoda pentaschista A. Gray. Field anoda, (DS).

Bastardia viscosa (C. Linnaeus) K. Kunth. Viscid bastardia, (BG).
Billietumera helleri (J. Rose ex A. A. Heller) P. Fryxell. Coppery
false fanpetals, (DS).

M alvas t rum americanum (C. Linnaeus) J. Torrey. Rio Grande
falsemallow, malva loca, (DS, RT).

M alvas t rum coromandelianum (C. Linnaeus) C. Garcke. Three-lobe
false-mallow, (DS, RT).

Rhynchosida physocalyx (A. Gray) P. Fryxell. Spear-leaf beaked
fanpetals, (DS).

Sida abutifolia P. Miller. Spreading fanpetals, (DS).

Sida spinosa C. Linnaeus. Prickly fanpetals, (DS).

NYCTAGINACEAE

Acleisanthes obtusa (J. Choisy) P. Standley. Berlandier’s trumpets,
vine four o’clock, (BG).

NYMPHAEACEAE

Nymphaea elegans W. J. Hooker. Blue waterlily, (RT).
OLEACEAE

Forestiera angustifolia J. Torrey. Narrow-leaf elbowbush, desert
olive, panalero, (BG).

ONAGRACEAE

Oenothera speciosa T. Nuttall. Showy evening-primrose, amapola
del campo, (DS).

OXALIDACEAE

Oxalis dichondrifolia A. Gray. Pony foot-leaf woodsorrel, (TB, DS).
Oxalis stricta C. Linnaeus. Common yellow woodsorrel, (DS).

PASSIFLORACEAE

Passiflora foetida C. Linnaeus var. gossypifolia (N. Desvaux ex W.

THE TEXAS JOURNAL OF SCIENCE- VOL. 56, NO. 1, 2004

Hamilton) M.T. Masters. Cotton-leaf passionflower vine, corona de
cristo, (DS).

PHYTOLACCACEAE

Rivina humilis C. Linnaeus. Rouge-plant, pigeonberry, (BG).
PLANTAGINACEAE

Plantago rhodosperma J. Decaisne. Redseed plantain, (DS).
PLUMBAGINACEAE

Limonium carolinianum (T. Walter) N. Britton. Sea-lavender,
marsh-rosemary, (SF, CM).

POLYGONACEAE

Rumex chrysocarpus G. Moris. Amnastla dock, (RT).
PORTULACACEAE

Portulaca oleracea C. Linnaeus. Purslane, (DS).

Portulaca pilosa C. Linnaeus. Chisme, (DS).

Portulaca umbraticola K. Kunth. Crowned wingpod purslane, (DS).
Talinum aurantiacum G. Engelmann. Orange flameflower, (BG).

PRIMULACEAE

Anagallis arvensis C. Linnaeus. Scarlet pimpernel, (DS, I).
Samolus ebracteatus K. Kunth subsp. cuneatus (J.K. Small) R.
Kunth. Wedge-leaf brookweed, (RT).

RANUNCULACEAE

Clematis drummondii J. Torrey & A. Gray. Barbas de chivato, old
man’s-beard, (DS).

RHAMNACEAE

Condalia hookeri M. C. Johnston. Brasil, (BG).

Karwinskia humboldtiana (J. A. Schultes) J. Zuccarini. Coyotillo,
(BG).

Ziziphus obtusifolia (W. J. Hooker ex J. Torrey & A. Gray) A. Gray.
Lotebush, (BG).

RUBIACEAE

Spermacoce glabra A. Michaux. Smooth false buttonweed, (RT).

LONARD, RICHARDSON & RICHARD

RUTACEAE

Zanthoxylum fagara (C. Linnaeus) C. Sargent. Colima, lime
pricklyash, (BG).

SALICACEAE

Salix nigra H. Marshall. Black willow, (RT).

SAPOTACEAE

Sideroxylon celastrinum (K. Kunth) T. Pennington. La coma, (BG).
SCROPHULARIACEAE

Bacopa monnieri (C. Linnaeus) F. Pennell. Coastal water-hyssop,
(RT).

Leucophyllum frutescens (J. Berlandier) I. M. Johnston. Cenizo,
(BG).

Mecardonia procumbens (P. Miller) J. K. Small. Yellow-flowered
mecardonia, (RT).

Veronica peregrina C. Linnaeus subsp. x alapensis (K. Kunth) F.
Pennell. Purslane speedwell, (RT).

SIMAROUBACEAE

Castela erecta P. Turpin subsp. texana (J. Torrey & A. Gray) J.
Rose. All-thorn goatbush, amargosa, (BG).

SOLANACEAE

Calibrachoa parviflora (A. L. de Jussieu) W. D’Arcy. Wild petunia,
(DS, I).

Capsicum annuum C. Linnaeus var. aviculare (J. Dierbach) W.
D’Arcy & W. Eshbaugh. Chilipiquin, (BG).

Chamaesaracha coronopus (M. Dunal) A. Gray. False nightshade,
(DS)..

Lycium berlandieri M. Dunal. Berlandier ’s wolfberry, (BG).
Lycium carolinianum T. Walter var. quadrifidum (M. Dunal) C.
Hitchcock. Coastal wolfberry, (RT, SF, CM).

Margaranthus solanaceus D. von Schlechtendal. Netted globeberry,
(DS).

Physalis cinerascens (M. Dunal) A. Hitchcock var. cinerascens
Ground cherry, (DS).

Physalis pubescens C. Linnaeus. Downy groundcherry, (DS).
Solanum americanum P. Miller. American black nightshade, (RT,
DS).

THE TEXAS JOURNAL OF SCIENCE— VOL. 56, NO. 1, 2004

Solarium campechiense C. Linnaeus. Red-berry nightshade, (RT).
Solarium elaeagnifolium A. Cavanilles. Silver-leaf nightshade,
trompillo, (DS).

Solarium triquetrum A. Cavanilles. Texas nightshade, (DS).
STERCULIACEAE

Melochia pyramidata C. Linnaeus. Angle-pod broomweed, (BG,
RT).

TAMARICACEAE

Tamarix aphylla (C. Linnaeus) G. Karsten. Athel tamarisk, (DS, I).
ULMACEAE

Celtis pallida J. Torrey. Spiny hackberry, granjeno, (BG).
URTICACEAE

Parietaria pensylvanica G. H. Muhlenberg ex C. von Willdenow.
Pellitory, (DS).

Urtica chamaedryoides F. Pursh. Heart-leaf stinging nettle, (RT,
DS).

VERBENACEAE

Aloysia gratissima (J. Gillies & W.J. Hooker) N. Troncoso. White
brush, (BG).

Glandularia bipinnatifida (T. Nuttall) T. Nuttall. Dakota mock
vervain, (DS).

Glandularia quadrangulata (A. A. Heller) R. Umber. Gulf coast
mock vervain, (DS).

Lantana achyranthifolia R. Desfontaines. Desert lantana, (BG).
Lantana urticoides A. von Hayek. Texas lantana, (BG, DS).

Phyla nodiflora (C. Linnaeus) E. Greene. Texas frog-fruit, (RT,
DS).

Verbena brasiliensis J. Velloso de Miranda. Brazilian vervain, (DS,

I).

Verbena canescens K. Kunth. Gray vervain, (DS).

Verbena halei J.K. Small. Texas vervain, (DS).

Verbena runyonii H. Moldenke. Runyon’s vervain, (DS).

VISCACEAE

Phoradendron tomentosum (A.P. de Candolle) G. Engelmann ex A.
Gray. Mistletoe, (BG).

LONARD, RICHARDSON & RICHARD

VITACEAE

Cissus incisa C. Des Moulins. Possumgrape, (DS).

LILIOPSIDA (MONOCOTS)

AGAVACEAE

Agave americana C. Linnaeus. Century plant, (DS).

Yucca treculeana E. Carriere. Spanish dagger, palma pita, (BG).

ALISM AT ACEAE

Echinodorus beteroi (K. Sprengel) N. Fasset. Beaked burhead,

CRT).

Sagittaria longiloba G. Engelmann ex J. Torrey. Long-lobe
arrowhead, (RT).

ALLIACEAE

Nothoscordum bivalve (C. Linnaeus) N. Britton. Crow-poison, (BG,
DS).

AMARYLLIDACEAE

Cooperia sp. Rainlily, (BG, DS).

BROM ELI ACEAE

Tillandsia bailey i J. Rose ex J.K. Small. Bailey’s ball moss, (BG,
TOES V. Watch list).

Tillandsia recurvata (C. Linnaeus) C. Linnaeus. Ball moss, (BG).
COMMELINACEAE

Callisia micrantha (J. Torrey) D. Hunt. Small-flowered roseling,
(BG).

' Commelina erecta C. Linnaeus var. angustifolia (A. Michaux) M.
Fernald. Widow’s tears, (DS).

CYPERACEAE

Bolboschoenus maritimus (C. Linnaeus) E. Pallasubsp .paludosus (A.
Nelson) T. Koyama. Prairie bulrush, (RT).

Cy perns articulatus C. Linnaeus. Jointed flat-sedge, (RT).

Cy perns esculentus C. Linnaeus. Yellow nutgrass, (RT).

Cyperus retroflexus S. Buckley. Backward- flexed flat-sedge, (DS).
Cyperus sp. Flat-sedge, (DS).

Eleocharis acicularis (C. Linnaeus) J.J. Roemer & J.A. Schultes.

THE TEXAS JOURNAL OF SCIENCE— VOL. 56, NO. 1, 2004

Needle spikerush, (RT).

Eleocharis austrotexana M.C. Johnston. South Texas spikerush,
(RT).

LEMNACEAE

Lemna minuta K. Kunth. Least duckweed, (RT).

POACEAE (Gramineae)

Aristida purpurea T. Nuttall var. longiseta (E. von Steudel) G.
Vasey. Red threeawn, (DS).

Bothriochloa laguroides (A.P. de Candolle) W. Herter subsp.
torreyana (E. von Steudel) K. Allred & F. Gould. Torrey’s silver
beard-grass, (BG).

Bouteloua trifida G. Thurber. Red grama, (BG).

Buchloe dactyloides (T. Nuttall) G. Engelmann. Buffalo-grass, (BG).
Chloris barbata O. Swartz. Bearded windmill-grass, (DS).

Chloris ciliata O. Swartz. Fringed windmill-grass, (DS).

Chloris x subdolichostachya J.K. A. Muller. Nash’s windmill-grass,
(BG, DS).

Cynodon dactylon (C. Linnaeus) C. Per soon. Bermuda-grass, (DS,

I).

Dichanthium annulatum (P. Forsskal) O. Stapf. Kleberg’s bluestem,
(DS, I).

Dichanthium aristatum (J. Poiret) C. Hubbard. Angleton bluestem,
(DS, I).

Dichanthium sericeum (R. Brown) A. Camus. Silky bluestem, (DS,

I).

Digitaria califomica (G. Bentham) J. Henrard. California cottontop,
(BG).

Digitaria pubiflora (G. Vasey) J. Wipff. Carolina crab-grass, (BG).
Enteropogon chlorideus (J. Presl) W. Clayton. Bury-seed
umbrella-grass, (BG).

Eragrostis reptans (A. Michaux) C. Nees von Esenbeck. Creeping
love-grass, (RT).

Eriochloa pseudoacrotricha (O. Stapf ex Thellung) C. Hubbard ex
S.T. Blake. Mock hairy-end cupgrass, (RT, DS, I).

Eriochloa punctata (C. Linnaeus) N. Desvaux ex W. Hamilton.
Spotted cup- grass, (RT).

Leptochloa dubia (K. Kunth) C. Nees von Esenbeck. Green
sprangletop, (BG).

Leptochloa Jusca (C. Linnaeus) K. Kunth subsp. uninervia (J. Presl)
N. Snow. Mexican sprangletop, (RT).

LONARD, RICHARDSON & RICHARD

Leptochloa nealleyi G. Vasey. Neally’s sprangletop, (RT).
Leptochloa panicea (A. Retzius) J. Ohwi subsp. brachiata (E. von
Steudel) N. Snow. Sprangletop, (DS).

Monanthochloe littoralis G. Englemann. Shore-grass, (SF, CM).
Panicum hallii G. Vasey var .filipes (L. Lamson-Scribner) F. Waller.
Filly panicum, (BG).

Pap pop ho rum vaginatumS. Buckley. Whip-lash pappus-grass, (BG).
Paspalidium geminatum (P. Forsskal) O. Stapf. Egyptian

paspalidium, (RT).

Paspalum denticulatum K. von Trinius. Long-tom, (RT).

Paspalum pubiflorum F. Ruprecht ex E. Fournier. Hairyseed

paspalum, (DS).

Pennisetum ciliare (C. Linnaeus) J. Link. Buffel-grass, (DS, I).
Setaria leucopila (F. Lamson-Scribner & E. Merrill) K. Schumann.
Plains bristle-grass, (BG).

Spartina spartinae (K. von Trinius) E. Merrill ex A. S. Hitchcock.
Gulf cord-grass, (CM).

Sporobolus pyramidatus (J. de Lamarck) A.S. Hitchcock. Whorled
drop-seed, (DS, SF).

Sporobolus virginicus (C. Linnaeus) K. Kunth. Sea-shore drop-seed,
(SF, CM).

Trichloris pluriflora E. Fournier. Multi- flowered false Rhode’ s-grass,
(BG).

Tridens albescens (G. Vasey) E. Wooton & P. Standi ey. White
tridens, (BG).

Tridens eragrostoides (G. Vasey) & F. Lamson-Scribner) G. Nash.
Love-grass tridens, (BG).

Tridens texanus (S. Watson) G. Nash. Texas tridens, (BG).
Urochloa fasciculata (O. Swartz) R.D. Webster. Brown- top

liver-seed grass, (DS).

Urochloa maxima (N. von Jacquin) R.E. Webster. Guinea grass,
(DS, I).

Urochloa panicoides A. Palisot de Beauvois. Panic liver-seed grass,
(A federally listed noxious weed, DS, I).

Urochloa texana (S. Buckley) R. D. Webster. Texas millet, (DS).
PONTEDERIACEAE

Heteranthera dubia (N. von Jacquin) C. MacMillan. Water stargrass,
(RT).

TYPHACEAE

Typha domingensis C. Persoon. Narrow-leaf cat-tail, (RT).

THE TEXAS JOURNAL OF SCIENCE- VOL. 56, NO. 1, 2004

The flora of PANBHS represents about one- fourth (24.2%) of the
total flora (1,004 species) of the Rio Grande Delta and the lower Rio
Grande Valley. Seven hundred thirty- two species of dicots representing
410 genera and 92 families were catalogued by Richardson (1995) in the
Rio Grande Delta. The Asteraceae (115 species), Fabaceae (74 species),
and Euphorbiaceae (47 species) are the most common families, and they
represent almost one- third (32.2%) of the species richness. Richardson
(1995) and Lonard (1993) listed 17 families, 99 genera and 269 species
of monocots. The Poaceae (188 species) and Cyperaceae (41 species)
account for 85.1% of the species richness of monocots in the area.

No rare, threatened, or endangered species were catalogued. How¬
ever, Tillandsia bailey i, epiphytic on Chloroleucon ebano in an upland
brush thicket, is listed as a category V "watch list" plant by the Texas
Organization for Endangered Species. Britton & Morton (1989) listed
Lycium carolinianum var. quadrifidum only along bay shores in Texas.
However, it was common in resaca basins and salt flats.

Several introduced potentially invasive grasses including Dichanthium
annulatum, Dichanthium aristatum, Pennisetum ciliare , Urochloa
maxima and Urochloa panicoides, occur in the core battlefield site and
in disturbed sites along roads and trails. Urochloa panicoides is a
federally listed noxious weed. No plans have been formulated to elimi¬
nate these species. Kalanchoe delagoensis is confined to a small area
near a parking lot and could be removed by hand.

Historical accounts indicate that S. spartinae was the most important
species in the core battlefield in 1846 (Sanchez 1985). Optimal develop¬
ment of a Gulf Cordgrass community occurs in saline, hydric soils
where water levels range from 30 cm below the soil surface to 4 cm
above ground level (Oefinger & Scifres 1977; Scifres et al. 1980).
Periodic flooding of the Rio Grande has been eliminated by dams and
drainage projects. Only occasional flooding occurs at PANBHS as a
result of rainfall rather than flooding from the river. Implementation of
a plan to restore S. spartinae at the battlefield site will require removal
of excess sediment from resaca channels, and cyclic flooding will be a
prerequisite to restore hydrologic processes. Therefore, it is doubtful
that the core battlefield can be restored to a landscape similar to condi¬
tions that prevailed in 1846.

LONARD, RICHARDSON & RICHARD

Acknowledgments

The authors thank the staff at the Palo Alto Battlefield National
Historic Site for granting permission to conduct this study. We are
indebted to Glennis Lonard for assistance in the collection of field data
and technical support.

Literature Cited

Blair, W. F. 1950. The biotic provinces of Texas. Texas J. Sci., 2(1):93-1 17.

Britton, J. C. & B. Morton. 1989. Shore Ecology of the Gulf of Mexico. Univ. of Texas
Press, Austin, 387 pp.

Brown, L. F., Jr., J. L. Brewton, TJ. Evans, J.H. McGovern, W. A. White, C. G. Groat
& W. L. Fisher. 1980. Environmental geological atlas of the Texas coastal
zone-Brownsville-Harlingen area. Univ. of Texas at Austin, Bureau of Economic
Geology, 140 pp.

Clover, E. U. 1937. Vegetational survey of the lower Rio Grande Valley, Texas.
Madrono, 4(1 ,2):41-72, 77-100.

Diamond, D. D., D. H. Riskind & S. L. Orzell. 1987. A framework for plant community
classification and conservation in Texas. Texas J. Sci., 39 (3):203-221.

Johnston, M. C. 1955. Vegetation of the Aeolian Plain and associated features of southern
Texas. Unpublished Ph.D. dissertation., Univ. of Texas at Austin, Austin, Texas, 167

pp.

Johnston, M. C. 1963. Past and present grasslands of southern Texas and northeastern
Mexico. Ecology, 44(3): 456-466.

Jones, S.D. & J. K. Wipff. 2003. A 2003 Updated Checklist of the Vascular Plants of
Texas. Botanical Research Center, Bryan, TX, 712 pp. (CD-ROM).

Kuchler, A. W. 1964. Potential Natural Vegetation of the Conterminous United States.

Special Publication 36. American Geographical Society, New York, 116 pp.

Lonard, R. I., J. H. Everitt & F. W. Judd. 1991. Woody Plants of Lower Rio Grande
Valley, Texas. Misc. Publ. No. 7. Texas Memorial Museum. Univ. Texas at Austin,
179 pp.

Lonard, R. I. 1993. Guide to Grasses of the Lower Rio Grande Valley, Texas. Univ. of
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Lonard, R. I. & F. W. Judd. 2002. Riparian vegetation of the lower Rio Grande.
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MacRoberts, M. H. & B. R. MacRoberts. 2003. West Gulf Coast Plain ecoregions. Sida,
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Oefinger, R. D. & C. J. Scifres. 1977. Gulf cordgrass production, utilization and
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Richardson, A. 1995. Plants of the Rio Grande Delta. Univ. of Texas Press, Austin, 332

pp.

Sanchez, J. P. 1985. General Mariano Arista at the Battle of Palo Alto, Texas 1846:

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RIL at: rlonard@panam.edu

TEXAS J. SCI. 56(l):35-54

FEBRUARY, 2004

SPATIAL AND TEMPORAL ABIOTIC CHANGES
ALONG A CANOPY TO INTERCANOPY GRADIENT
IN CENTRAL TEXAS JUNIPERUS ASHEI WOODLANDS

Rob Wayne and O. W. Van Auken

Center for Water Research
University of Texas at San Antonio
San Antonio, Texas 78249

Abstract . -Juniperus ashei (ashe juniper), in the southern Edwards Plateau region of
central Texas, exhibits both spatial and temporal trends in seedling demography, emergence,
growth and physiology which vary in relation to patterns of woodland overstory: the canopy
patches of woody plants vs. the intercanopy patches of grasses and herbs between them.
This study reports gradients of abiotic factors found from below J. ashei canopy trees into
associated intercanopy patches. There were significant differences in soil organic content,
soil field capacity, soil temperature, soil water content and surface light levels along this
gradient from April through December 1997, but not soil depth. Mean soil organic content
was highest under the canopy (32.0 ± 6.9%) and lowest in the intercanopy patch (12.5 ±
0.8%) as was the field capacity (108.5 ± 2.8% and 82.9 ± 1.6% respectively). Mean mid¬
day light levels were highest in the intercanopy (1183 ± 149 /xmol • m'2 • s'1) and were lowest
below the canopy (346 ± 99 /xmol • m'2 • s'1 and 219 ± 77 /xmol • m'2 • s'1, canopy and mid¬
canopy respectively). Mean midday soil temperature varied seasonally, but was highest in
the intercanopy (32.6 + 2.1°C) and lowest at the canopy edge (27.6 ± 1.4°C). Mean soil
water content also varied seasonally (with rainfall), and was highest under the canopy (43.4
± 3.0%) and lowest in the intercanopy (30.3 ± 2.1%). Reduced light levels under the
canopy, coupled with high soil organic content may ameliorate high soil temperatures and
promote higher soil water content, possibly resulting in reduced water stress and increased
J. ashei seedling survival. However, increased growth at the canopy edge may be attributed
to increased surface light levels at this location. Low seedling emergence and survival in the
intercanopy patch may be due to a combination of factors, in particular seasonal high soil
surface temperatures and low soil water content.

The Edwards Plateau of central Texas comprises approximately 10
million hectares (Gould 1975; Diamond et al. 1995). It is bordered on
the north by the High Plains and Rolling Plains, on the west by the
Trans-Pecos Region, and on the southern and eastern boundaries by the
Balconies Escarpment. In many parts of the Edwards Plateau, especially
in the southern portion, Juniperus ashei is a dominant woodland species
(Van Auken et al. 1981; Van Auken 1988). Juniperus ashei co-occurs
with Quercus fusiformis {— Q. virginiana , Hatch et al. 1990), Q. texana
and Diospyros texana in these woodlands (Van Auken et al. 1981).

Juniperus ashei is an evergreen aromatic shrub or small tree ( < 9 m)
with one or several trunks (Correll & Johnson 1979); it is fire sensitive
(Foster 1917; Johnson & Alexander 1974; Fuhlendorf et al. 1996) and
likely drought tolerant (Fonteyn et al. 1985; Wayne & Van Auken

THE TEXAS JOURNAL OF SCIENCE- VOL. 56, NO. 1, 2004

2002) . Densities of J . ashei in these woodlands in the southern part of
the Edwards Plateau are * 1500 trees/ha (Van Auken et al. 1981; Van
Auken 1988) with an estimated canopy cover of 40 to 90% (Van Auken
et al. 1981; Smeins & Merrill 1988). Car ex planostachys (cedar sedge)
occurs under the Juniperus canopy and is an herbaceous species with
high cover and wide distribution in these woodlands (Wayne 2000).

These central Texas Juniperus woodlands are fairly open in some
places and are associated with glades or small grasslands (Quarterman
1950; Baskin & Baskin 1978, 2000; Quarterman et al. 1993; Terletzky
& Van Auken 1996). These open areas are more correctly referred to
as intercanopy patches (Breshears et al. 1997a; 1997b; Martens et al.
1997; Reid et al. 1999; Van Auken 2000a; Ware 2002). Additionally,
these intercanopy patches may have a high or low cover of herbaceous
plants which appears to be related to soil depth (Terletzky & Van Auken
1996; Van Auken 2000a).

Juniperus ashei was present historically in the southern Edwards
Plateau region (Foster 1917; Diamond et al. 1995), in areas that offered
protection from grassland fires such as steep rocky slopes or outcrops.
However, J. ashei , like many other woody species, has increased its
density in grasslands over the past 100 to 150 years (Bray 1904; Foster
1917; Diamond 1997; Scholes & Archer 1997; Brown & Archer 1999).
Causes of this encroachment are likely due to continuous, heavy grazing
by domestic herbivores leading to reduced light fluffy fuel and decreased
fire frequency (McPherson et al. 1988; Riskind & Diamond 1988;
Diamond et al. 1995; Fuhlendorf et al. 1996; Van Auken 2000b).
Anthropogenic factors such as elevated levels of C02 and climatic
change are often cited (see Polley et al. 1996) as possible causes of
woody plant encroachment, but are not necessary to explain these
community changes (Archer et al. 1995; Van Auken 2000b). It is
unknown if J. ashei is continuing to encroach into the remaining
intercanopy patches, but predictive models indicate that grasslands are
maintained with frequent fires (Fuhlendorf et al. 1996).

The physiology and demography of J . ashei in central Texas
woodlands and intercanopy patches is poorly understood. Mature 7.
ashei trees exhibit low stomatal conductance and carbon assimilation
during summer drought (Owens & Schreiber 1992; Owens 1996) and
high water stress (Fonteyn et al. 1985; Wayne & Van Auken 2002).
These trends are reversed in the fall through spring when temperatures
are lower and the soil water content is higher. Density of J. ashei

WAYNE & VAN AUKEN

seedlings in these woodlands appear to be influenced by spatial and
temporal gradients of abiotic factors (Wayne & Van Auken 2002).

In addition, seedling emergence is highest in early winter through
early spring; with most emergences occurring beneath the woodland
canopy (Jackson & Van Auken 1997), a smaller number of seedling
emergences occur at the canopy edge and few in the inter canopy patch.
Most J. ashei seedling mortality coincides with summer drought, with
the highest mortality in the intercanopy patch, followed by the canopy
edge and lowest mortality below the canopy (Jackson & Van Auken
1997; Van Auken et al. 2004). Seedling growth rates on the other hand
are highest at the canopy edge and reduced under the canopy. Juniperus
ashei seedling water stress is highest during summer drought (< -7.0
MPa), but recovers quickly with small rainfall events (Wayne & Van
Auken 2002). Juniperus ashei seedlings at the canopy edge exhibit
greater water stress than canopy seedlings during summer drought, but
no data is available for seedlings in the intercanopy patches. Carex
planostachys, a co-occurring sub-canopy herbaceous species appears to
have a water stress response similar to that of J. ashei seedlings (Wayne
2000).

Although several studies have described plant communities in various
parts of the Edwards Plateau Region (Van Auken et al. 1981; Van
Auken 1988; Terletzky & Van Auken 1996; Van Auken 2000a) none
have reported the cause of differences in J. ashei seedling survival or
growth, but have suggested various abiotic factors. Van Auken (2000a)
reported the presence of a soil depth gradient. Wayne & Van Auken
(2002) indicated a xylem water potential gradient in J. ashei woodlands.
It is hypothesized that gradients of other abiotic factors occur. These
gradients may be responsible for the variation in species density and
cover in these Juniperus woodlands. The purpose of this study is to
quantify the magnitude and direction of the abiotic gradients from
beneath the J. ashei canopy into the intercanopy.

Materials and Methods

This study was conducted April through December 1997 on a 1760
m2 site in Eisenhower Park, a San Antonio, Texas city park, in northern
Bexar County (98°34’26” W and 29°37’19” N), located on the southern
Edwards Plateau. The park is 128 ha and maintained as a natural area
without domestic grazing (> 50 yrs, Eric Lautzenheiser pers. comm.).
The site is near the Balconies fault zone and approximately 5 km east of
the University of Texas at San Antonio campus. A site was selected
representative of a J. ashei woodland with an associated intercanopy

THE TEXAS JOURNAL OF SCIENCE- VOL. 56, NO. 1, 2004

patch that appeared to be infrequently accessed by humans. Soil is a
clayey-skeletal, smectitic, thermic lithic calciustoll (United States
Department of Agriculture 2000) in the Tarrant association - rolling -
with a slope of 4.5° to 13.5°. Three horizons occur that consist of
shallow, clayey, weakly calcareous soil, developed over hard limestone
with scattered stones and gravel. The surface horizon ranges from 0 cm
to 25 cm in thickness. The subsurface is approximately 20 cm thick,
heavily fractured limestone over limestone bedrock (Taylor et al. 1962).
Regional climate is classified as subtropical - subhumid with a mean
annual temperature of 20°C (Arbingast et al. 1976). Monthly mean
temperature ranges from 9.6°C in January to 29.4°C in July (National
Oceanic and Atmospheric Administration 1999). Annual precipitation
in the study area is 78.7 cm, with two peaks occurring in May and
September with monthly means of 10.7 cm and 8.7 cm, respectively.
During the study, precipitation was above normal for 1997 at 85.6 cm
(National Oceanic and Atmospheric Administration 1999), with a low of
0.0 cm in July, negligible in August, and a high of 18.5 cm in June.

The area vegetation is juniper/oak woodland representative of similar
woodlands found throughout this region (Van Auken et al. 1981). The
predominant woody vegetation is J. ashei and Quercus virginiana (live
oak). Other woody species reported from the area are Q. texana
(Spanish oak), Celtis laevagata (hackberry), Diospyros texana (Texas
persimmon), Berberis trifoliata (agarita) and Rhus virens (evergreen
sumac) (Van Auken et al. 1980; 1981; Terletzky & Van Auken 1996).
Car ex planostachys (Correll & Johnston 1979) was the dominant herba¬
ceous species below the woodland canopy. The major herbaceous
species in the inter canopy patches were Aristida longiseta (red
three-awn), Bouteloua curtipendula (side-oats gramma), other C3 and C4
grasses and a variety of herbaceous annuals (Fowler & Dunlap 1986;
Van Auken 2000a).

Measurements of surface and subsurface soil moisture, soil tempera¬
ture, soil organic content and field capacity were made at each of five
positions along six parallel northeasterly transects (41° azimuth).
Frequency and time of measurements are indicated for each factor. The
surface horizon of the soil was the upper 2 cm of soil and the subsurface
horizon was the lowest 2 cm of soil adjacent to the bedrock. Each
transect was 15 m in length and at least 3 m from an adjacent transect.
A plumb line dropped from the outermost branch of mature 7. ashei
trees (2 m above the ground, located directly above each transect) was
used to locate the canopy edge (drip line). Surveyor tapes were used to
establish the following sampling positions: 10 m inside the canopy

WAYNE & VAN AUKEN

(canopy), 5 m inside the canopy (mid-canopy), 0 m inside the canopy
(canopy edge), 2.5 m outside the canopy (mid- inter canopy) and 5 m
outside the canopy (intercanopy). There were 6 transects by 5 sampling
positions for the surface horizon and for the subsurface horizon.
Significant differences in soil moisture and soil temperature were
detected between the surface and subsurface horizons (ANOVA, SAS
Institute 1989). Because the overall mean values between the surface
and subsurface were small (< 2°C for soil temperature and < 5% for
soil moisture) surface measurements will be the main focus of this
paper.

Soil moisture was determined using the gravimetric procedure and
reported as the percent water in the sample on a dry-mass basis (Pearcy
1989; United States Department of Agriculture 1996; Jackson et al.
2000). Soil samples were collected along each transect (n = 6), at each
position (n = 5) for the surface and bedrock horizons (n = 2) in April,
May, July, August, September, October, and twice in December (n =
8 for a total of 480 samples). Stones and organic litter were removed
from the soil surface; soil samples were collected and sealed in plastic
bags for transport to the lab. Approximately 40 g of soil was placed in
a pre-weighed aluminum planchet, weighed and oven dried at 100°C to
a constant mass.

Soil temperature was measured within two hours after solar noon on
the same dates as soil moisture (with the exception of May and the latter
December measurement (n = 6 months for a total of 360 samples) using
15 cm long, probe type, analog soil thermometers (Broadbent 1965;
Larcher 1995). Surface temperature was measured by inserting the
probe 1 to 2 cm into the soil and recording the temperature after five
minutes of equilibration. Subsurface temperature was measured by
excavating soil to the bedrock and inserting the probe into the lowest 2
cm of exposed soil.

Surface light levels (photosynthetically active photon flux density, X
= 400 to 700 run,) were measured at solar noon on cloudless days in
July, August, October and December (n = 4 months for a total of 120
samples) with a LI-COR® (LI-COR Inc., Lincoln, Nebraska) LI- 190 SA
integrating quantum sensor. Light levels were recorded with a LI-COR®
LI- 1000 data logger in instantaneous mode with 60 s averaging at 5 s
intervals. No measurements were made April through June 1997
because of overcast conditions. The quantum sensor was placed level
on bare ground at each position and no attempt was made to move or
disrupt any woody or herbaceous vegetation over the sensor.

THE TEXAS JOURNAL OF SCIENCE- VOL. 56, NO. 1, 2004

The soil depth profile was measured at the conclusion of this study to
minimize potential disturbances to the plants and soil of the study area
(Broadbent 1965). Surface litter was removed and measurements were
made along each transect at 0.5 m intervals ( n = 186) using a 60 by 1
cm rebar driven vertically into the ground until it would not penetrate
any deeper. The distance from the top of the rod to the ground was
measured and subtracted from 60 cm to obtain the soil depth. Periodic¬
ally, the rebar was re- measured to ensure the length did not change.

Percent soil organic content was determined for the surface and
bedrock horizons (n = 2 for a total of 60 samples) using the loss-on-
ignition procedure (Broadbent 1965; United States Department of Agri¬
culture 1996). Excess soil collected from the December 1997 soil mois¬
ture sampling was used for the determination of the soil organic content.
The soil was air-dried and sieved (#10 mesh), tested for the presence of
carbonates (United States Department of Agriculture 1996), oven dried
at 90 °C and incinerated in a Fischer Muffle Furnace (Model 58) at
600 °C for 3 hours. The test for presence of carbonates was negative.

Determination of percent field capacity (Broadbent 1965) for the
surface and bedrock horizon was made using sieved (#10 mesh), air-
dried soil, however only four transects were utilized (n = 2 for a total
of 40 samples). The soil was placed level into a perforated aluminum
planchet lined with # 1 filter paper, thoroughly wetted for 12 h and
drained for 20 minutes. The soil was then oven dried to a constant mass
at 100°C.

The experimental design was factorial for surface light, soil water and
soil temperature (position by date). Data were transformed as needed
prior to statistical analysis and analyzed with ANOVA (SAS Institute
1989). When significant main effects were detected, data were subset
to examine temporal and spatial differences using ANOVA and the
Scheffe multiple comparison test (a = 0.05, SAS Institute 1989). Mean
surface values were pooled temporal data (all dates) for each transect
position to show the overall spatial differences in surface values.
Although ANOVA may indicate that a significant difference occurred the
Scheffe multiple comparison test may indicate otherwise because of its
conservative nature in computing the minimum significant difference
(three examples occurred, SAS Institute 1989; Sokal & Rohlf 1995).

Results

Soil depth was erratic and did not vary significantly from the canopy
to the intercanopy patch ( F = 0.69, P = 0.8858, Fig. 1). Mean soil
depth (+ SE) ranged from 9.9 ± 2.3 cm under the full canopy to 7. 1

WAYNE & VAN AUKEN

c/>

-15 -10 -5 0 5 10

TRANSECT POSITION (m)

Figure 1. Mean soil depth profile (surface to bedrock, cm) measured at 0.5 m intervals
along the canopy to intercanopy gradient (n = 6 transects) in the Juniperus ashei
woodland. Lower bar with dotted line is an example standard error bar. Transect
position (x-axis) is in meters from the canopy edge: canopy (-10), mid-canopy (-5),
canopy edge (0), mid-intercanopy (2.5) and intercanopy (5). P- value for the AN OVA
indicated no significant difference in positions.

-15 -10 -5 0 5 10

TRANSECT POSITION (m)

Figure 2. Spatial differences in mean (± SE) percent soil organic content and percent field
capacity at the surface horizon. P-values indicated are for individual ANOVA’s. Transect
position (x-axis) is in meters from the canopy edge: canopy (-10), mid-canopy (-5),
canopy edge (0), mid-intercanopy (2.5) and intercanopy (5). Means within a measured
parameter with different letters are significantly different (Scheffe multiple comparison
test) .

± 2.1 cm at the canopy edge and 10.6 ± 3.1 cm in the intercanopy
patch. Soil depth ranged from zero to 40 cm and the overall mean depth
was 9.2 ± 2.5 cm.

Overall mean soil organic content varied significantly by position (F
= 8.59, P = 0.0001) and ranged from 32.0 ± 6.9% under the full
canopy (Fig. 2) to 16.8 ± 2.6% at the canopy edge and 12.5 + 0.8%

THE TEXAS JOURNAL OF SCIENCE— VOL. 56, NO. 1, 2004

TRANSECT POSITION (m)

Figure 3. Yearly mean (± SE) surface gradient (n = 6 transects) from below the Juniperus
canopy into the intercanopy (n = 5 positions) for (a) surface light levels (junol • m"2 • s'1)
and (b) surface soil temperature (°C) and surface soil moisture (%). Light levels were
measured at solar noon on cloudless days in July, August, October and December 1997
(n = 4). Soil temperature was measured within two hours after solar noon in April, July,
August, September, October and December ( n = 6). Soil moisture was measured in
April, May, July, August, September, October and twice in December (n = 8). Transect
position (x-axis) is in meters from the canopy edge: canopy (-10), mid-canopy (-5),
canopy edge (0), mid-intercanopy (2.5) and intercanopy (5).

in the intercanopy patch. The Scheffe multiple comparison test indicated
there was a significant difference in mean soil organic content between
the canopy position and both patch positions, but no significant differ¬
ence between the mid-canopy and the canopy edge positions.

Overall field capacity varied significantly by position (F = 31.90, P
= 0.0001) and ranged from 108.5 + 2.8% under the Juniperus wood¬
land canopy (Fig. 2) to 81.3 ± 2.9% at the canopy edge and 82.9 ±
1.6% in the intercanopy. The Scheffe multiple comparison test indicated
that there was not a significant difference between the canopy and mid-

WAYNE & VAN AUKEN

Table 1. F-tables and significance levels from three separate analyses of variance, examining
(a) light levels, (b) soil temperature and (c) % soil moisture. Variables examined include
the overall model, date (D), transect position (P), soil horizon (H) and the various two
and three-way interactions. Transect positions are canopy, mid-canopy, canopy edge,
mid-intercanopy patch and intercanopy patch. * = P < 0.05, ** = P < 0.01, *** =
P < 0.001, **** = P < 0.0001 and NS = not significantly different.

(a) Light levels.

(b) Soil temperature.

Source

Model

6.67****

Model

36.90****

Model

23.77****

Date (D)

13.92****

Date (D)

365.00****

Date (D)

7 218.81****

Position (P) 4

16.37****

Horizon (H) 1

78.55****

Horizon (H)

1.32ns

D*P

1.62NS

Position (P) 4

19.80****

Position (P)

39 28****

D*H

2.69*

D*H

9.99****

D*P

8.38****

D*P

5.66***

H*P

0.88ns

H*P

2.86****

H*d*P

0.49ns

H*D*P

0.53ns

canopy positions but they differed from all other positions. There was
no significant difference between means for the canopy edge and the
intercanopy positions.

The overall trend in surface light levels, soil temperature and soil
moisture are best observed by pooling all surface temporal data for each
position (Fig. 3). Mean surface light levels varied significantly by date
and position, but the interaction term was not significant (Table la).
Spatially, surface light levels (Fig. 3a) were lowest below the canopy
and mid-canopy positions, 346 ± 99 /xmol • m"2 • s'1 and 219 ± 77
fxmol • m'2 • s'1 respectively, were intermediate at the canopy edge and
highest in the intercanopy (1183 ± 149 fjanol • m2 • s'1) . Mean soil
temperature varied significantly by date, horizon, and position, with two
significant two-way interactions (Table lb). The significant interactions
were date by horizon and date by position, but the three-way interaction
was not significant. Spatially, mean yearly surface temperatures (Fig.
3b) were lowest at the canopy edge (27.6 ± 1.4°C), intermediate below
the canopy (29.5 ± 1.8°C) and highest in the intercanopy (32.6 ±
2.1°C). Mean soil moisture varied significantly by date and position,
with 3 significant two-way interactions (Table lc). The three-way inter¬
action was not significant. The general spatial trend for surface soil
moisture (Fig. 3b) was highest values below the canopy (43.4 ± 3.0%),
intermediate values at the canopy edge (33.6 ± 2.2%) and lowest values
in the intercanopy (30.3 ± 2.1%).

Surface light below the canopy did not vary significantly (F = 1.98,

THE TEXAS JOURNAL OF SCIENCE- VOL. 56, NO. 1, 2004

Figure 4. Temporal change in mean (± SE) surface light levels (jnmol«m'2*s‘‘, n = 6
transects) below the canopy, at the canopy edge and in the intercanopy. Surface light was
measured at solar noon on cloudless days in July, August, October and December 1997
(i n = 4). Significance levels are indicated to the right of each position in the legend: NS
is not significantly different, * is P < 0.05.

P > 0.05) and ranged from 675 ± 309 /xmol • m'2 • s'1 in July (Fig. 4) to
39 ± 7 /xmol • m2 • s1 in December. At the canopy edge, surface light
varied significantly (F = 3.37, P < 0.05) and ranged from 666 ± 307
/xmol •m‘2«s"1 in July to 78 ± 17 /xmol • m*2 • s"1 in December; however,
the Scheffe multiple comparison test did not detect any significant
differences between dates. In the intercanopy, surface light varied signi¬
ficantly (F = 6.88, P < 0.05) ranging from 1614 ± 302 /xmol • m2- s"1
in July to 479 + 225 /xmol • m"2 • s"1 in December. The August mean of
1531 ± 243 /xmol • m'2 • s'1 was significantly different from the October
and December means (Scheffe multiple comparison test), but not the
July mean.

Temporal differences in mean surface temperature below the canopy
varied significantly (F = 41.37, P = 0.0001) and ranged from 25.6 ±
1 .9°C in May (Fig. 5a) to a high of 46.5 ± 3.3°C in August and a low
of 16.0 ± 0.3°Cin December. Mean surface temperature at the canopy
edge varied significantly (F = 53.83, P = 0.0001) and ranged from
25.6 ± 0.7°C in May, increased to a high of 39.8 ± 2.2°C in July and
a low of 16.3 ± 1.0°C in December. In the intercanopy, mean surface
temperature varied significantly (F = 32.66, P = 0.0001) from 31.0 ±
0.7 °C in May to a high of 48.8 ± 1.0°C in July and a low of 18.1 ±
0.8°C in December. Surface soil temperatures followed air tempera¬
tures (with a lag) and were high in July and August, and low in

WAYNE & VAN AUKEN

a :
D
H

6-Mar 25-Apr 14-Jun 3-Aug 22-Sep 11 -Nov 31 -Dec

MONTH-1997

Figure 5. Temporal change in (a) mean (± SE) surface soil temperature (°C, n = 6
transects) and (b) mean (± SE) surface soil moisture (%, n = 6 transects) below the
canopy, at the canopy edge and in the intercanopy. Temperature measurements were
made within two hours after solar noon in April, July, August, September, October and
December 1997 ( n = 6). Soil moisture was measured in April, May, July, August,
September, October and twice in December ( n = 8). Significance levels are indicated
to the right of each position in the legend: * is P = 0.0001.

December. The highest surface soil temperature was 48.8 ± 1.0 °C in
July in the intercanopy and the lowest was in December at 16.0 ±
0.3°C under the canopy. A significant decline from the high soil
temperatures seen in July and August for all positions occurred in early
September (« 12 °C), coinciding with a 0.8 cm precipitation on the day
preceding temperature measurements. After September soil temperature
continued a significant decline to the low values observed in December
for all positions except the intercanopy.

Temporal differences in mean surface soil moisture varied signifi-

THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 1, 2004

cantly below the canopy (F = 16.94, P = 0.0001) and ranged from

68.4 ± 7.0% in May (Fig. 5b) to a low of 18.9 ± 2.1% in July. Fol¬
lowing the September precipitation, soil moisture increased to 52.2 ±
2.1%, followed by a second, but significant decline, and subsequent
significant increase to 55.6 ± 6.8% after a late December precipitation
event. The canopy edge and intercanopy locations also varied signifi¬
cantly (F = 42.5, P = 0.0001 and F = 84.2, P = 0.0001) and with the
same significant decreases and increases seen below the canopy location.
The canopy edge was at 47.7 ± 3.8% in May, decreased to a low of

12.5 ± 1.7% in August, increased to 39.5 ± 1.5% in September and
was at 51.0 ± 2.4% in December. In the intercanopy, mean soil
moisture was 43.2 ± 3.3% in May, declined to 6.8 + 0.4% in July,
increased to 38.6 ± 2.3% in September and was at 43.2 ± 2.0% in
December. The overall temporal trend was high surface soil moisture
in April-May and low surface soil moisture in June-August.

Discussion

Soil depth in this study did not indicate a gradient from canopy to
intercanopy locations. The very erratic soil depth observations from the
Juniperus woodland canopy into the intercanopy patch were likely due
to numerous surficial bedrock fractures (Davenport et al. 1996). At the
northeastern extent of 7. asheV s range, calcareous derived soils are
prevalent with rock outcrops common as well as fractures and pockets
of deep soil (Quarterman et al. 1993; Ware 2002). These findings in 7.
ashei woodlands are not unlike those of Pinus edulus /Juniperus
monosperma communities of New Mexico where soil depth fluctuated
from 33 to 125 cm over distances of 10 m and without any significant
differences between canopy and intercanopy locations (Davenport et al.
1996). Other 7. monosperma communities such as those in Arizona
(Johnsen 1962) and 7. pinchotii in north Texas (McPherson et al. 1988)
also occur over fractured bedrock. A similar trend of shallow soils over
fractured bedrock has been reported for other locations in the Edwards
Plateau (Foster 1917; Taylor et al. 1962; Owens & Schreiber 1992).
However, gradients of soil depth have been reported in open patch
communities in central Texas (Van Auken 2000a) and deeper soils have
been confirmed in woodlands compared to intercanopy patches in this
same area (Terletzky & Van Auken 1996; Ware 2002).

Specific spatial abiotic gradients were found during this study for soil
organic content, field capacity, surface light levels, soil temperature and
soil water content. The general trend was a decrease in soil organic

WAYNE & VAN AUKEN

content, field capacity, and soil water content from beneath the
Juniperus canopy into the intercanopy patch. Surface light and soil
temperature followed a reverse trend with high surface light levels and
high soil temperatures in the intercanopy patch and lower values beneath
the woodland canopy. Temporal differences in surface light, soil
temperature and soil moisture were not presented for the mid-canopy
and mid- inter canopy positions. However it was noted when examining
individual dates the mid-canopy differed little from the canopy, and the
mid-intercanopy differed little from the intercanopy (see Wayne 2000).

While surface litter, derived from the overstory, was not measured
during this study it does have an influence on soil moisture content as
it is incorporated into the soil (Knapp et al. 1993; Breshears et al.
1997b). It was noted that surface litter at the study site was ~ 3 - 5 cm
thick below the canopy, thin at the canopy edge, and absent in the inter¬
canopy. In addition, the trend in soil organic content appears to coin¬
cide with areas of litter deposition and greater litter depth. High
amounts of organic matter have a direct relationship with the soil water
holding capacity and soil field capacity (Bel sky & Canham 1994;
Larcher 1995; Jackson et al. 2000). An additional characteristic of
surface litter is that it insulates the soil from atmospheric temperature
(Knapp et al. 1993; Breshears et al. 1998). It was demonstrated that
soil organic content was low or absent in the intercanopy and increased
from the canopy edge into the full canopy position. Similar trends in
soil organic content and litter have been noted in African savannas with
high levels found proximal to overstory trees (Belsky et al. 1989; 1993).
In addition, the same has been found in J. pinchotti communities on the
northern Edwards Plateau (Dye 1993; Dye et al. 1995) and west Texas
(McPherson et al. 1991), pinon/juniper communities in New Mexico
(Davenport et al. 1996) and other savanna communities (Belsky &
Canham 1994).

Surface light levels were reduced beneath the Juniperus woodland
likely due to light interception by the overstory canopy. This light
reduction has been reported in other J. ashei communities on the
Edwards Plateau (Yager & Smeins 1999), in oak savannas on the
Edwards Plateau (Anderson et al. 2001), in J. monosperma communities
in New Mexico (Breshears et al. 1997b; 1998; Martens et al. 2000) and
in J . virginiana communities in the eastern North America (Joy &
Young 2002). In pinon/juniper communities, differences in surface light
levels are related mainly to canopy/ intercanopy patch variation (i.e.,
overstory/no overstory) (Breshears et al. 1997b). Differences in light

THE TEXAS JOURNAL OF SCIENCE- VOL. 56, NO. 1, 2004

levels are not only spatial trends but temporal trends as well; and spatial
effects are modified temporally. Light levels in pinon/juniper
communities varied less temporally beneath the canopy than in the
intercanopy patch, but the observed temporal differences were greatest
during summer and least during winter. In J. ashei communities (this
study), the spatial /temporal trends in light levels are similar to those
reported in the Juniperus communities in New Mexico. Temporally
light was highest during summer and reduced in winter. Light levels
were higher in the intercanopy patch, intermediate at the canopy edge
and lower in the canopy positions, which is consistent with pinon/juniper
communities in western North America.

Soil temperatures from the canopy to the inter canopy patch followed
a trend similar to the surface light gradient, lower soil temperatures
below the canopy and highest temperatures in the intercanopy patch.
This is consistent with J. monosperma communities in New Mexico
(Breshears et al. 1997a) and J. virginiaia communities in eastern North
America (Joy & Young 2002). Reduced canopy soil temperature is
probably related to the interception of light by the canopy reducing
heating of the soil by solar radiation (Helgerson 1990; Belsky et al.
1993; Breshears et al. 1997b). In addition, surface litter probably
provides insulation of the soil from atmospheric temperature (Knapp et
al. 1993; Breshears et al. 1998). Conversely, the higher soil tempera¬
tures in the intercanopy patch are influenced by the lack of overstory
shading and absence of surface litter (Breshears et al. 1998). Soil
moisture was also higher below the Juniperus canopy and may also play
a role in the reduced canopy soil temperatures. High soil moisture also
appears to ameliorate high soil temperatures across the entire gradient
as noted following small precipitation events (Berndtsson et al. 1996;
Wayne & Van Auken 2002).

A specific temporal trend of variable soil temperature was also
detected. Peak soil temperatures across the study site were reached in
late August; these high temperatures were subsequently modified, ~
20 °C, by a small precipitation event (0.8 cm) in early September
followed by a continued seasonal decline, ~ 10°C, from fall through
winter. In addition, during fall and winter there was little difference in
mean soil temperature along the gradient (see Wayne 2000). Pinon/
juniper woodlands in New Mexico followed a similar temporal trend
where soil temperatures were elevated in the intercanopy patch (relative
to the canopy) during the summer and decline fall through winter
(Breshears et al. 1998). Differences were attributed to seasonal air

WAYNE & VAN AUKEN

temperatures and the changing angle of the sun.

Trends in soil moisture along the canopy to intercanopy patch gradient
were reversed from that described for surface soil temperatures, soil
moisture was highest below the canopy and reduced in the intercanopy
patch. The exception to this trend was noted after precipitation events
when differences between positions were not apparent. Possible causes
for differences in soil moisture have been mentioned previously; includ¬
ing the canopy intercepting light resulting in reduced soil temperatures
and also the high litter content below the canopy further ameliorating
evaporative loss (Yager & Smeins 1999; Anderson et al. 2001; Joy &
Young 2002).

Some pinon/juniper woodlands (Breshears et al. 1997a; 1997b; 1998)
and oak savannas (Anderson et al. 2001) have lower soil moisture below
the canopy and canopy edge then the adjacent patch, but it is unclear
whether this was due to canopy interception of rainfall and/or evapo-
transpiration. With regard to pinon/juniper woodlands the soil moisture
trend varies with time such that either patch type, canopy or inter¬
canopy, can have increased soil moisture at some point during the year
(Breshears et al. 1997b). Thus, these central Texas Juniperus wood¬
lands were dissimilar from those in New Mexico that had mostly higher
soil moisture in the intercanopy. High soil organic content and litter
cover below the canopy may account for greater water storage capacity
(measured as field capacity, Fig. 2). Runoff during rainfall from small
intercanopy areas into canopy areas (Wilcox 1994; Ware 2002) may also
increase soil moisture below the canopy and redistribute sediment (and
litter) from the intercanopy into the canopy (Reid et al. 1999). Tem¬
porally, soil moisture was found to be decreased from spring into
summer after cessation of rainfall (from ~ 53% to 13% soil moisture),
but recharge occurred rapidly (from ~ 13% to 44% soil moisture) after
small precipitation events (Wayne 2000; Wayne & Van Auken 2002).

Throughout most of the year abiotic conditions at the canopy edge are
intermediate (see Wayne 2000; Wayne & Van Auken 2002) to the
canopy and patch positions. Differences in aboveground canopy cover
appear to explain a considerable amount of the heterogeneity detected in
abiotic factors along the gradients in these Juniperus woodlands
(Breshears et al. 1997b). Soil depth was not significantly different in
this study and does not seem to play a role in the abiotic gradients.
Higher J . ashei seedling emergence and survival (Jackson & Van Auken
1997; Van Auken et al. 2004), and high predawn xylem water potential

THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 1, 2004

below the canopy (Wayne & Van Auken 2002) seems related to the
reduced stress attributable to slightly lower soil temperature and higher
soil moisture. Thus, the canopy likely facilitates J. ashei in the early
stages of its growth and development (Callaway et al. 1996; Joy &
Young 2002). However, the canopy may also hinder J. ashei seedling
growth due to light interception and reduced surface light levels
(McKinley & Van Auken 2004), more so below the full canopy position
then at the canopy edge.

Reduced availability of water and increased soil temperature appears
to hinder seedling emergence and survival, while at the same time the
increased light likely promotes seedling growth (Van Auken et al. 2004).
This anomalous statement appears to explain differences in survival and
growth of 7. ashei seedlings in these different positions along the
gradient. The intercanopy position exhibited the greatest soil
temperature and lowest soil moisture, which seems to explain the low
emergence and survival of J . ashei seedlings at this position along the
gradient. Small precipitation events during late summer also appears to
be important in reducing water stress of J. ashei , and other drought
tolerant herbaceous species (see Wayne 2000) in these Juniperus com¬
munities (Fonteyn et al. 1985; Wayne & Van Auken 2002).

Acknowledgements

The authors wish to thank E. Lautzenheiser and others with the City
of San Antonio Parks and Recreation Department for their cooperation,
and for permission to carry out this study in Eisenhower Park. The
support of W. and L. Collenback, through a generous scholarship to the
senior author is most appreciated. In addition, grants provided by the
University’s College of Science and Engineering, and the Division of
Life Science to the senior author helped make this work possible. Last¬
ly, we wish to thank the Center for Water Research for their support in
publishing this work.

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RW at: erwayne@utsa.edu

TEXAS J. SCI. 56(l):55-62

FEBRUARY, 2004

REPRODUCTIVE CYCLE OF THE SIDEWINDER,
CROTALUS CERASTES (SERPENTES: VIPERIDAE),

FROM CALIFORNIA

Stephen R. Goldberg

Department of Biology, Whittier College
Whittier, California 90608

Abstract. — Reproductive tissue was examined from 159 museum specimens of Crotalus
cerastes from California. Males follow a seasonal testicular cycle with sperm produced
June-October; regressed testes were present March-June and October. Timing of this cycle
is similar to that of other North American rattlesnakes. Sperm were present in the vasa
deferentia March-October. Mean litter size for 26 C. cerastes was 7.96 ± 2.9 SD, range
= 3-14. The number of females that were gravid (enlarged follicles > 8 mm or oviductal
eggs) during the April to August period of female reproductive activity was 28/53 (53%).
The presence of females with early yolk deposition in April and May when other females
were gravid suggests more than one reproductive season is needed to complete yolk
deposition.

The sidewinder, Crotalus cerastes , ranges from southern Nevada,
southern California, south-central Arizona and extreme southwestern
Utah, south to northeastern Baja California and northwestern Sonora; it
occurs from below sea level to around 1830 m and is most common
where there are sand hummocks topped with creosote bushes or mes-
quite (Stebbins 2003). Information on reproduction in C. cerastes is
summarized in Ernst & Ernst (2003). Reiserer (2001) reported on
reproduction in C. cerastes but did not perform gonadal histology. The
purpose of this paper is to provide information on the reproductive cycle
of C. cerastes from California from a histological examination of gonads
from museum specimens.

Material and Methods

Sixty-two female (mean snout- vent length, SVL = 486 mm ± 53 SD,
range = 375-592 mm) and 97 male (mean SVL = 446 mm ± 53 SD,
range = 331-543 mm) C. cerastes were borrowed from the herpetology
collections of the Natural History Museum of Los Angeles County, Los
Angeles, California and the San Diego Society of Natural History, San
Diego, California. Snakes were collected during 1935-1977. The left
testis and part of the vas deferens were removed from males; the left
ovary was removed from females for histological examination. Enlarged
follicles (> 8 mm length) or oviductal eggs were counted; no histology

THE TEXAS JOURNAL OF SCIENCE— VOL. 56, NO. 1, 2004

was done on them. Tissues were embedded in paraffin and cut into
sections at 5 /xm. Slides were stained with Harris’ hematoxylin, fol¬
lowed by eosin counter stain. Testes slides were examined to determine
the stage of the spermatogenic cycle; vasa deferentia were examined for
the presence of sperm. Ovary slides were examined for the presence of
yolk deposition (= secondary vitellogenesis sensu Aldridge 1979a).
Numbers of specimens examined by reproductive tissue were: testis =
97, vas deferens = 75, ovary = 34. The relationship between SVL and
litter size was investigated by regression analysis. Unpaired r-tests were
used to compare C. cerastes male and female mean body sizes (SVL),
mean litter sizes with those from Klauber (1972), and mean litter sizes
of northern versus southern populations from Klauber (1972).

Material examined.— Specimens of Crotalus cerastes from California
(by county) examined from the herpetology collection of the Natural
History Museum of Los Angeles County, Los Angeles (LACM) and the
San Diego Society of Natural History (SDSNH). IMPERIAL: (LACM)
9202-9204, 52575, 52576, 64024, 104487, 104489, 104490. INYO: 52572,
104491, 116013, 116014; (SDSNH) 3219. KERN: (LACM) 52577, 52578,
63628, 63629, 63631, 63638, 63640-63642, 63644, 69905, 104493, 104495,
137690. LOS ANGELES: (LACM) 28006, 52579, 63447. RIVERSIDE:
(LACM) 3025, 19936, 19938, 19942, 19944, 19945, 23235, 27996, 27998,
28000, 28001, 28783, 52582, 104499, 104500, 104507, 104508, 104511,
104512, 104519, 104523, 104542, 104547, 104549, 104552, 104555, 104557,
104560-104565, 104569, 104572, 104578, 104580, 104586, 104589, 104595,
104597, 104601, 104610, 104611, 104619, 104630, 104634, 104641, 104647,
104654, 104665, 104668, 104675, 104677, 104689, 104690, 104692, 104713,
104726, 104735, 104738, 104862, 116002, 1 16004, 1 16007, 116008, 123762,
138215; (SDSNH) 31929, 33096, 39296, 39301, 39302. SAN BERNAR¬
DINO: (LACM) 3018, 19919, 19921, 19922, 19924, 21908, 63632, 63634,
63643, 63645, 63647-63649, 70262, 70265, 70266, 70269, 104750, 104757,
104762, 104768, 104770, 104772, 104776, 104782, 104783, 104785, 104787,
104788, 104790-104793, 104796-104798, 116011, 116012, 125994, 132244;
(SDSNH) 25397, 31758. SAN DIEGO: (LACM) 28002-28005, 76300,
104799, 104805, 104806, 104809, 104810, 104813, 125997, 126295.

Results and Discussion

Testicular histology was similar to that reported by Goldberg &
Parker (1975) for two colubrids Masticophis taeniatus and Pituophis
catenifer ( = P. melanoleucus) and the viper id Agkistrodon piscivorus by
Johnson et al. (1982). In the regressed testis, seminiferous tubules

GOLDBERG

Table 1. Monthly distribution of reproductive conditions in seasonal testicular cycle of
Crotalus cerastes. Values are the numbers of males exhibiting each of the three
conditions.

Month

Regression

Recrudescence

Spermiogenesis

March

April

May

June

July

August

September

October

contained spermatogonia and Sertoli cells. There was a proliferation of
germ cells; primary and secondary spermatocytes and occasional
spermatids were present in testes undergoing recrudescence. During
spermiogenesis, seminiferous tubules were lined by spermatozoa. Rows
of metamorphosing spermatids were also present.

Monthly stages in the testicular cycle are shown in Table 1 . Males
undergoing spermiogenesis were present June to October; males with
regressed testes were present in March-June and October. Reiserer
(2001) found maximum testes sizes of C. cerastes occurred during
September. Males with testes in recrudescence were present March to
August. The presence of males undergoing spermiogenesis during
summer and autumn indicates C. cerastes has a testicular cycle similar
to those of other North American rattlesnakes in which sperm formation
occurs during this period (Aldridge 1979b; Aldridge & Brown 1995;
Goldberg 1999a, 1999b, 1999c, 2000a, 2000b, 2000c, 2002; Goldberg
& Holycross 1999; Goldberg & Rosen 2000; Holycross & Goldberg
2001; Goldberg & Beaman 2003). This pattern of spermatogenesis fits
the "aestival spermatogenesis" of Saint Girons (1982). Sperm were
present in 74/75 (99%) of the vasa deferentia examined: March 8/9,
April 27/27, May 21/21, June 3/3, July 4/4, August 4/4, September
3/3, October 4/4. The smallest mature male, LACM 104783 (regressed
testis; sperm in vas deferens from previous spermiogenesis) measured
331 mm SVL (360 mm total length, TL). This is less than the smallest
male (49.5 mm TL) found in copulation by Secor in Ernest (1992).
Field observations have indicated C. cerastes mates both in spring
(Klauber 1972; Brown & Lillywhite 1992) and fall (Lowe 1942).

THE TEXAS JOURNAL OF SCIENCE- VOL. 56, NO. 1, 2004

Table 2. Monthly distribution of reproductive conditions in seasonal ovarian cycle of
Crotalus cerastes. Values shown are the numbers of females exhibiting each of the four
conditions.

Month

Inactive

Early yolk
deposition

Enlarged follicles
(> 8 mm width)

Oviductal

eggs

January

February

March

April

May

20*

June

July

August

September

October

* Includes two females with damaged eggs; litters could not be reliably estimated.

Reiserer (2001) reported both spring and fall matings in captive C.
cerastes. A captive pair of C. cerastes mated 1 1 October (Klauber
1972).

Mean female body size (SVL) was significantly larger than that of
males ( t = 4.73, df = 157, P < 0.0001). Reiserer (2001) similarly
found female C. cerastes to be generally larger than the same-aged
males. Crotalus cerastes may be the only species of North American
Crotalus in which females are larger than males (Ernst 1992), however
further study will be needed before this is known. Monthly stages in the
ovarian cycle are shown in Table 2. Females with enlarged follicles ( >
8 mm length) or oviductal eggs were present April to August. Reiserer
(2001) reported ovulation in C. cerastes occurred during late June. The
smallest reproductively active female (follicles > 8 mm length) (LACM
104549) measured 383 mm SVL (408 mm TL). This value is less than
the 434 mm TL recorded for the smallest gravid C. cerastes female in
Klauber (1944). There was no significant difference between the mean
litter size (7.96 + 2.9 SD, range = 3-14, n = 26) for C. cerastes in
this study and the mean litter size in Klauber (1972) (9.5 ± 3.0 SD ,
range = 5-18, n = 38 ) t = 2.0, df = 62, P = 0.05. Litters may
contain 1-20 young, but typically have 7-12 (Ernst & Ernst 2003). Fitch
(1985), using data from Klauber (1972), reported mean litter sizes of
10.8 ± 0.1 SE, range: 7-18 for 10 C. cerastes from the Mohave Desert
(northern) and 9.0 + 0.5 SE, range: 5-16 for 28 from the Colorado

GOLDBERG

Table 3. Litter sizes for Crotalus cerastes from California.

Date

SVL (mm)

Litter size

County

LACM ft

20 April 1961

485

Riverside

104552

27 April 1958

395

Riverside

104668

28 April 1962

560

Riverside

104738

3 May 1963

421

Riverside

104547

3 May 1963

451

Riverside

104578

4 May 1968

514

Riverside

116004

4 May 1968

528

Riverside

104713

5 May 1968

522

Kern

63644

5 May 1963

530

Riverside

28000

6 May 1961

522

Riverside

104619

7 May 1967

445

Los Angeles

52579

11 May 1974

435

Riverside

138215

16 May 1963

563

Kern

69905

16 May 1965

400

Riverside

104542

18 May 1966

509

Imperial

9203

19 May 1958

560

Riverside

104862

20 May 1961

435

Riverside

104630

20 May 1961

495

Riverside

104508

23 May 1958

438

Riverside

104595

24 May 1958

498

San Bernardino

104790

24 May 1963

383

Riverside

104549

12 June 1961

483

Riverside

104511

15 June 1960

463

Riverside

104500

27 July 1962

490

San Bernardino

21908

5 August 1968

498

San Diego

125997

15 August 1954

459

Riverside

3025

* Contained oviductal eggs; others contained enlarged follicles > 8 mm length.

Desert and Arizona (southern). There was no significant difference
between mean litter sizes of these northern versus southern C. cerastes
populations (t = 1.7, df = 36, P = 0.10). Examination of additional
samples from other areas will be needed to ascertain the degree of
geographic variation in C. cerastes litter sizes.

Litter sizes for 26 gravid C. cerastes females are given in Table 3.
Regression analysis (Fig. 1) revealed a significant positive correlation
between In (litter size) and In (SVL) for these 26 litters: (In litter size =

THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 1, 2004

Figure 1 . Linear regression of enlarged follicles ( > 8 mm length) or oviductal eggs on
snout- vent length, mm (log transformed variables) for 26 Crotalus cerastes females from
California (regression equation in text).

-8.34 + 1.68 In SVL) r2 = 0.19, P = 0.024. Back transformed this
regression equation describes the allometric relationship via a power
function: litter size = e'8 34SVL* 68 (King 2000).

The number of gravid females (enlarged follicles > 8 mm or
oviductal eggs) during the April to August period of female reproductive
activity was 28/53 (53%). The presence of non-reproductive females
(Table 2) during the period when other C. cerastes females are gravid
indicates that not all females reproduce each year. This has been
reported for other western North American rattlesnakes (Goldberg
1999a, 1999b, 1999c, 2000a, 2000b, 2000c, 2002; Goldberg & Holy-
cross 1999; Goldberg & Rosen 2000; Holycross & Goldberg 2001;
Rosen & Goldberg 2002). The frequency of reproduction in female
rattlesnakes is unknown but is likely influenced by available food
reserves (Goldberg & Rosen 2000; Rosen & Goldberg 2002). Long¬
term field studies will be required before the frequency of female
reproduction can be known for C. cerastes.

The presence of C. cerastes females with early yolk deposition in
April and May when other females were gravid (Table 2) suggests yolk
deposition and ovulation are completed over more than one reproductive
season and may be approximately biennial. Biennial reproduction may
be "typical" for many species of North American rattlesnakes with the

GOLDBERG

likelihood of less frequent reproduction during years of low food
availability, and the potential of reproduction in successive years when
food is abundant.

Acknowledgments

I thank D. Kizirian (LACM) and B. Hollingsworth (SDSNH) for
permission to examine specimens.

Literature Cited

Aldridge, R. D. 1979a. Female reproductive cycles of the snakes Arizona elegans and
Crotalus viridis. Herpetologica, 35(3):256-261.

Abridge, R. D. 1979b. Seasonal spermatogenesis in sympatric Crotalus viridis and Arizona
elegans in New Mexico. J. Herpetol., 13(2): 187-192.

Aldridge, R. D. & W. S. Brown. 1995. Male reproductive cycle, age at maturity, and cost
of reproduction in the timber rattlesnake ( Crotalus horridus). J. Herpetol.,
29(3): 399-407.

Brown, T. W. & H. B. Lilywhite. 1992. Autecology of the Mojave desert sidewinder,
Crotalus cerastes cerastes , at Kelso Dunes, Mojave Desert, California, USA. Pp.
279-308, in Biology of the Pitvipers. (J.A. Campbell and E.D. Brodie, Jr., eds.), Selva,
Tyler, Texas, xi + 467 pp.

Ernst, C. H. 1992. Venomous reptiles of North America. Smithsonian Institution Press,
Washington, ix + 236 pp.

Ernst, C. H. & E. M Ernst. 2003. Snakes of the United States and Canada. Smithsonian
Books, Washington, ix 4- 668 pp.

Fitch, H. S. 1985. Variation in clutch and litter size in New World reptiles. Univ. Kansas
Mus. Nat. Hist., Misc. Publ., 76:1-76.

Goldberg, S. R. 1999a. Reproduction in the tiger rattlesnake, Crotalus tigris (Serpentes:
Viperidae). Texas J. Sci., 51(l):31-36.

Goldberg, S. R. 1999b. Reproduction in the blacktail rattlesnake, Crotalus molossus
(Serpentes: Viperidae). Texas J. Sci., 5 1(4): 323-328.

Goldberg, S. R. 1999c. Reproduction in the red diamond rattlesnake in California. Calif.
Fish and Game, 85 (4): 177- 180.

Goldberg, S. R. 2000a. Reproduction in the twin-spotted rattlesnake, Crotalus pricei
(Serpentes: Viperidae). West. North Am. Nat., 60(1):98-100.

Goldberg. S. R. 2000b. Reproduction in the rock rattlesnake, Crotalus lepidus (Serpentes:
Viperidae). Herpetol. Nat. Hist., 7(l):83-86.

Goldberg, S. R. 2000c. Reproduction in the speckled rattlesnake, Crotalus mitchellii
(Serpentes: Viperidae). Bull. Southern Calif. Acad. Sci., 99(2): 101-104.

Goldberg, S. R. 2002. Reproduction in the Arizona black rattlesnake, Crotalus viridis
cerberus (Viperidae). Herp. Nat. Hist., 9(l):75-78.

Goldberg, S. R. & A. T. Holycross. 1999. Reproduction in the desert massasauga,
Sistrurus catenatus edwardsii, in Arizona and Colorado. Southwestern Nat.,
44(4):531-535.

Goldberg, S. R. & W. S. Parker. 1975. Seasonal testicular histology of the colubrid
snakes, Masticophis taeniatus and Pituophis melanoleucus . Herpetologica,
3 1 (3) :3 17-322.

THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 1, 2004

Goldberg, S. R. & P. C. Rosen. 2000. Reproduction in the Mojave rattlesnake, Crotalus
scutulatus (Serpentes: Viperidae). Texas J. Sci., 52(2): 101-109.

Goldberg, S. R. & K. R. Beaman. 2003. Reproduction in the Baja California rattlesnake,
Crotalus enyo (Serpentes: Viperidae). Bull. Southern Calif. Acad. Sci., 102(1 ): 39-42.

Holycross, A. T. & S. R. Goldberg. 2001. Reproduction in northern populations of the
ridgenose rattlesnake, Crotalus willardi (Serpentes: Viperidae). Copeia, 2001(2):473-481.

Johnson, L. F., J. S. Jacob & P. Torrance. 1982. Annual testicular and androgenic cycles
of the cottonmouth (Agkistrodon piscivorous) in Alabama. Herpetologica, 38(1): 16-25.

King, R. B. 2000. Analyzing the relationship between clutch size and female body size in
reptiles. J. Herpetol., 34(1): 148-150.

Klauber, L. M. 1944. The sidewinder, Crotalus cerastes, with description of a new
subspecies. Trans. San Diego Soc. Nat. Hist., 10(8):91-126.

Klauber, L. M. 1972. Rattlesnakes. Their habits, life histories and influence on mankind.
2nd edit., Vol. 1, University of California Press, Berkeley, xlvi + 740 pp.

Lowe, C. H., Jr. 1942. Notes on the mating of desert rattlesnakes. Copeia,
1942(4): 26 1-262.

Reiserer, R. S. 2001. Evolution of life histories in rattlesnakes. Unpublished Ph.D.
dissertation, Univ. Calif. Berkeley, xxii -I- 256 pp.

Rosen, P. C. & S. R. Goldberg. 2002. Female reproduction in the western diamond-backed
rattlesnake, Crotalus atrox (Serpentes: Viperidae), from Arizona. Texas J. Sci.,
54(4): 347-356.

Saint Girons, H. 1982. Reproductive cycles of male snakes and their relationships with
climate and female reproductive cycles. Herpetologica, 38(1 ) :5- 1 6.

Stebbins, R. C. 2003. A field guide to western reptiles and amphibians, 3rd edit., Houghton
Mifflin Company, Boston, Massachusetts, xiii + 533 pp.

SRG at: sgoldberg@whittier.edu

TEXAS J. SCI. 56(l):63-72

FEBRUARY, 2004

FRESHWATER MUSSELS (BIVALVIA: UNIONIDAE)

OF THE VILLAGE CREEK DRAINAGE BASIN
IN SOUTHEAST TEXAS

Vickie L. Bordelon and Richard C. Harrel

Department of Biology
Lamar University
Beaumont, Texas 77710

Abstract.— A total of 18 species and 2,235 individuals of freshwater mussels were
collected from 22 sites in the Village Creek basin. The number of individuals per site ranged
from zero to 528 and the number of species per site ranged from zero to 13. Relative abun¬
dance for all collection sites varied from zero to 176 individuals/person-hours. Quadrula
mortoni and Fusconaia askewi comprised 60 percent of the total individuals collected and
relative abundance was 14.8 and 13.1 individuals/person-hours, respectively. Lampsilis
satura, Obovaria jacksoniana and Pleurobema riddellii were collected at several sites and
are listed as "of special concern" by the American Fisheries Society.

Freshwater mussels are good indicators of water quality and are often
the first organism to decline during adverse conditions (Rosenburg &
Resh 1993; Howells et al. 1996; Howells 1997). Howells et al. (1997)
reported that 52 species of freshwater bivalves occurred in Texas and
discussed 18 that were dramatically reduced in abundance. Williams et
al. (1993) listed 17 of these 52 species as threatened, endangered, or of
special concern. This survey of the freshwater bivalves of the Village
Creek drainage basin evaluates the current status of the populations and
will serve as a baseline reference for subsequent studies.

There has been no extensive study of the bivalves of Village Creek.
Strecker (1931) and Parks (1938) listed some bivalves that occurred in
Village Creek, but these works are dated and uncertainties in systematics
limit their present day use. Vidrine (1990) surveyed one location in
Village Creek for his study of parasitic mites of freshwater mussels.
Howells et al. (1996) listed some mussels known to have occurred in
Village Creek, but in a later paper (Howells 1997) on the status of
mussels in the Big Thicket region he mentioned an unsuccessful effort
by Texas Parks and Wildlife Department personnel to collect any living
mussels from Village Creek.

Several studies have been conducted on the physical/chemical condi¬
tions and macrobenthos of Village Creek and its tributaries (Tatum &
Commander 1971; Harrel 1977; Kost 1977; Lewis & Harrel 1978;

THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 1, 2004

Commander 1980; Newberry 1982; Harrel 1985; Barclay & Harrel
1985), but the sampling techniques were not adequate to survey the
bivalve fauna. Nearby Texas and Louisiana mussel surveys were con¬
ducted by Neck (1986), Feaster (1997), Howells (2000) and Vidrine
(2001).

Description of the Area

Village Creek is a 5th order stream located in Hardin, Tyler and Polk
counties in southeast Texas (Figure 1). From its origin, near the city of
Livingston in Tyler County, it flows southeasterly into the Neches
River. The basin drains an area of approximately 2,883 km2 and has an
axial length of 125 km. Land uses in the basin consist of lumber
production, several small municipalities (< 10,000 residents) and scat¬
tered residential developments. Some reaches of Village Creek and its
tributaries are within the boundaries of the Alabama- Coushatta Indian
Reservation, the Big Thicket National Preserve, Roy Larsen Nature
Conservancy Sanctuary and Village Creek State Park. The remaining
sections of the stem stream of Village Creek, from the Big Thicket
National Preserve Big Sandy Creek Unit to the confluence with the
Neches River are proposed as additions to the Big Thicket National
Preserve (Big Thicket National Preserve 1996).

The shallow substrate in the stream channel consisted of fine and
coarse sand with pockets of silt, detritus and clay. Sunken logs are
abundant. The average gradient is 0.38 m/km and the minimum and
maximum daily discharge based on 66 years of record was 1.8 m3/sec
and 131.6 m3/sec (USGS 2001). Dominant vegetation along the stream
banks consists of Taxodium distichum (bald cypress), Nyssa aquatica
(water tupelo), Betula nigra (river birch) and Quercus sp. (water tolerant
oaks) .

Methods

Twenty-two sites were sampled between 9 August 2001 and 25
November 2002 (Figure 1). Seventeen sites were located along the
lower stem stream and five sites were in smaller tributaries. Vidrine
(1998) reported that small to moderate size streams resulted in low to
moderate mussel diversity and larger, downstream reaches often had
higher diversity and larger populations. At each site, 1.5 to 3 person-
hours were spent hand- searching the substrate for mussels, covering an
average of 50 meters of shoreline. Vaughn (1995) and Hornbach &

BORDELON & HARREL

Figure 1 . The Village Creek drainage basin and locations of sites sampled (in the order in
which they were sampled).

Deneka (1996) stated that non-quantitative random time search methods
are preferred when examining the distribution of freshwater mussels.
Sampling was done only during relatively low stream discharge and
depth conditions as indicated by the U.S. Geological Survey gauging
station 08041500 located near Kountze, Texas (USGS 2001). Mean
water depth for all collecting dates was 1.2 m and mean discharge was
5.6 m3/sec. These conditions allowed productive sampling, which could
not have occurred at greater depth or discharge.

Living mussels collected were identified, counted and measured.
Most specimens were returned to the stream, but some were retained in
order to confirm identification or to be used as reference specimens.
Dead shell material was not documented. Retained specimens were
returned to the laboratory and placed in three percent ethyl alcohol to
cause the valves to gape, then preserved in 95 percent ethyl alcohol.
Identifications were made using the following taxonomic references;
Burch (1973), Cummings & Mayer (1992), McMahon (1991), Howells
et al. (1996) and Vidrine (2001). Robert Howells (Texas Parks and

THE TEXAS JOURNAL OF SCIENCE— VOL. 56, NO. 1, 2004

Table 1. Total number of living individuals of each species collected at each site sampled.
(Total number of person-hours spent = 48.)

Site

Amblema plicata

Fusconaia askewi

212

Fusconaia flava

Lampsilis hydiana

Lampsilis satura

Lampsilis teres

Leptodea fragilis

Obliquaria reflexa

Obovaria jacksoniana

Plectomerus dombeyanus

Pleurobema riddellii

Potamilus purpuratus

Quadrula mortoni

185

Quadrula nobilis

Toxolasma texasiensis

Tritogonia verrucosa

Uniomerus tetralasmus

Villosa lienosa

Total

111

152

528

109

130

Wildlife Department), verified the identifications. Common and
scientific names are those of Turgeon et al. (1998).

Voucher specimens were placed in a collection at Lamar University.
Relative abundance of all mussels for each collection site was calculated
by the formula: number of individuals of all species collected/person-
hours (48) spent collecting at that site. Relative abundance for each
species was determined by the formula: number of individuals of a
species collected/ total person-hours (48) for entire study.

BORDELON & HARREL

Table 1. (Continued)

Site

Ambletna plicata

Fusconia askewi

Fusconaia flava

Lampsilis hydiana

Lampsilis satura

Lampsilis teres

Leptodea fragilis

Obliquaria reflexa

Obovaria jacksoniana

Plectomerus dombeyanus

Pleurobema riddellii

Potamilus purpuratus

Quadrula mortoni

Quadrula nobilis

Toxolasma texasiensis

Tritogonia verrucosa

Uniomerus tetralasmus

Villosa lienosa

Total

128

109

126

117

120

106

Results and Discussion

During the study, 18 species of unionds and 2,235 individuals were
collected during a total of 48 person-hours (Table 1). The number of
species per collection site ranged from zero at site 9 to 13 at sites 1, 2
and 3 (Table 2). The number of individuals per collection site ranged
from zero (site 9) to 528 (site 3). No mussels were found at site 9 after
2.25 person-hours of searching. This was probably due to the unsuitable
habitat that was composed of steep cut clay banks and tree roots, which
made searching difficult. Relative abundance of all mussels at individual

THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 1, 2004

Table 2. Number of species collected, mussels collected, person-hours spent collecting, and
relative abundance for each collecting site. Data indicates living specimens only.

Site

Species

collected

Number

collected

Person-hours

Relative

abundance

111

152

528

176

109

130

2.50

2.25

0.4

128

109

126

1.5

117

1.5

120

106

1.5

collection sites ranged from zero (site 9) to 176 (site 3) per person-hour
(Table 2).

Site 3 had a large diversity of microhabitats including substrate types,
variations in flow, and a large area of suitable depth for collecting. Site
3 is the location where Vidrine (1990) collected and removed 1,000
individuals for his study of mites associated with mussels. Site 3 is also
the location where Texas Parks and Wildlife personnel reported finding
no living mussels (Howells et al. 1996). This was probably due to their
collecting method. They used a brail, which cannot be effectively
utilized in Village Creek due to the amount of sunken trees.

Quadrula mortoni and Fusconaia askewi were the most abundant
species, representing 31.8 and 28.2 percent, respectively, of the total
number of individuals collected during the study (Table 3). Relative
abundance of Q . mortoni and F. askewi was 14.8/person-hour and
13.1/person-hour, respectively. Quadrula mortoni occurred at 20
collecting sites and F. askewi occurred at 18 sites. These species are
euryecious and were found in all types of substrates and were often the
only species found in coarse sand away from the shore. One specimen

BORDELON & BARREL

Table 3. Total number of sites where species occurred, total number of individuals collected,
percentages of all individuals collected, and relative abundance of each species (in order
of relative abundance). Data indicates living specimens only.

Species

Site

frequency

Number

collected

% of total
collected

Relative

abundance

Quadrula mortoni

712

31.8%

14.8

Fusconaia askewi

631

28.2%

13.1

Lampsilis hydiana

170

7.6%

3.5

Amblema plicata

166

7.4%

3.5

Quadrula nobilis

135

6.3%

2.9

Fusconaia flava

101

4.5%

1.7

Toxolasma texasiensis

4.0%

1.9

Lampsilis teres

3.0%

1.4

Villosa lienosa

2.2%

1.0

Lampsilis satura

1.4%

Plectomerus dombeyanus

1.4%

Obovaria jacksoniana

<1%

Pleurobema riddellii

<1%

Leptodea fragilis

<1%

Tritogonia verrucosa

<1%

Potamilus purpuratus

<1%

Obliquaria reflexa

<1%

Uniomerus tetralasmus

<1%

<.l

of F. askewi measured 74 mm in shell length, which exceeds the
maximum length recorded for Texas waters (Howells et al. 1996).
Uniomerus tetralasmus was the least abundant species and was collected
only in two tributary streams; one specimen each in Beech Creek (site
12) and Turkey Creek (site 13). This species is adapted for desiccation,
dewatering and stagnant water (Neck & Metcalf 1988; Cummings &
Mayer 1992) and was the only species collected only in smaller tributary
streams.

Three species found during this study are listed as of "special
concern" by the American Fisheries Society (Williams et al. 1993).
These include Lampsilis satura, Obovaria jacksoniana and Pleurobema
riddellii. Only eight living specimens of L. satura had been reported in
the Big Thicket region during the past five years (Howells 1997).
During this study 33 specimens from seven sites were collected (Tables
1 & 3). Howells (1997) reported that only one dead shell of Obovaria
jacksoniana had been found in Texas since 1990. During this study, 16
specimens of O. jacksoniana were collected from four sites (Tables 1 &
3). Since 1987, only two living and two dead specimens of P. riddellii
have been reported from the central Neches River in Texas (Howells
1997). During this survey 1 1 specimens from four sites were collected
(Tables 1 & 3).

THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 1, 2004

Seven species of mussels were considered to be uncommon or rare
and represented less than one percent of the total number collected and
their relative abundance was less than 0.5 clams per person-hour (Table
3). Three species of mussels that were previously collected in Village
Creek or the nearby Neches River during benthic surveys, but not
during this study, include Glebula rotundata, Quadrula apiculata and
Megalonaias nervosa. The exotic Asiatic clam, Corbicula fluminea , was
noted at sites 1, 2, 4, 5, 8, 9, 11, 12, 13 and 20, but it was abundant
only at sites 11 and 13 in Turkey Creek.

The results of this study indicate that Village Creek supports a diverse
and healthy bivalve fauna. However, Neck (1982), Samad & Stanley
(1986), Alderman & Adams (1993), Layzer & Gordon (1993) Neves
(1993) and Howells (2000) reported that habitat alterations in and around
waterways adversely alter mussel habitats. Within the basin, current and
projected residential development and economic growth, together with
increased recreational usage of Village Creek, may effect bivalve popu¬
lations. The bivalve fauna should be monitored closely in the future to
ensure protection of these organisms.

Acknowledgments

This study was funded by a student research award from the Texas
Academy of Science to V. Bordelon and a Lamar University Scholar
award to R. Harrel.

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Neck, R. W. 1986. Freshwater bivalves of Lake Tawakoni, Sabine River, Texas. Tex. J.
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Neck, R. W. 1989. Freshwater bivalves of Arrowhead Lake, Texas: apparent lack of
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Missouri. Upper Mississippi River Conservation Committee, Rock Island, Illinois, 189

pp.

Newberry, W. 1982. Physicochemical conditions, fecal bacteria, and benthic macroinverte¬
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thesis, Lamar University, Beaumont, Texas, 89 pp.

THE TEXAS JOURNAL OF SCIENCE- VOL. 56, NO. 1, 2004

Parks, H. B. 1938. Mollusca. Pages 7-8, in H. B. Parks & V. L. Cory (eds.), Biological
Survey of the East Texas Big Thicket Area. Texas Agricultural Experiment Station,
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Rosenberg, D. M. & V. H. Resh. 1993. Introduction to freshwater biomonitoring and
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Baylor University Museum, Bulletin 2, 63 pp.

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Turgeon, D. D., A. E. Bogan, E. V. Coan, W. K. Emerson, W. G. Lyons, W. L. Pratt, C.
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VLB at: VBordelon@aol.com

TEXAS J. SCI. 56(1), FEBRUARY, 2004

GENERAL NOTES

NOTEWORTHY RECORDS OF THE MILLIPEDS,
EURYMERODESMUS ANGULARIS AND E. MUNDUS
(POLYDESMIDA: EURYMERODESMIDAE), FROM
NORTHEASTERN AND WESTCENTRAL TEXAS

Chris T. McAllister, Rowland M. Shelley* and Dawn I. Moore

Department of Biology, Texas A&M University-Texarkana
Texarkana, Texas 75505 and

^Research Laboratory, North Carolina State Museum of Natural Sciences
4301 Reedy Creek Road, Raleigh, North Carolina 27607

The milliped family Eurymerodesmidae occurs from northeastern
Nebraska, central Illinois and southeastern North Carolina to the Rio
Grande and north Florida, and is the dominant representative of the
order Polydesmida in the central United States (Shelley 1990). It is a
monotypic genus, but is relatively diverse with 25 known species.
Eurymerodesmus mundus Chamberlin has been reported from north¬
eastern Nebraska through eastern Oklahoma and southwestern Arkansas
to Cooke, Dallas, Grayson and Johnson counties, Texas, and E.
angularis Causey is known from southern Missouri, the Coastal Plain of
Arkansas, eastern Mississippi and northern Louisiana (Shelley 1990).
This study provides the first report of E. angularis from Texas and four
new records for E. mundus that significantly increase its known distribu¬
tion within the state.

Between October 2001 and May 2003, locations (primarily in State
Parks) within 24 Texas counties (Bosque, Bowie, Brown, Cass, Coryell,
Dallas, Delta, Fannin, Freestone, Harrison, Hopkins, Jack, Johnson,
Limestone, Marion, Morris, Parker, Red River, Shackleford, Somervell,
Taylor, Titus, Tom Green and Travis) and Caddo Parish, Louisiana,
were examined for millipeds in general and eurymerodesmids in particu¬
lar. Individuals were encountered primarily in damp spots off park trails
by overturning decaying logs and leaf litter with potato rakes. Occasion¬
al specimens were collected by peeling bark off fallen trees and rotting
stumps. At each locale, specimens were placed in individually labeled
vials containing 70% ethanol and returned to the laboratory for identifi¬
cation. Specimens were identified by examining the male genitalia. In
eurymerodesmids both the gonopods and gonopodal apertures in males
hold taxonomic utility as do the female cyphopods, which possess

THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 1, 2004

projections and other unique morphological features. Voucher speci¬
mens were deposited in the invertebrate collection of the North Carolina
State Museum of Natural Sciences.

Several specimens of E. mundus were found during the study period
in Texas; data are as follows:

Cass County, 8.1 mi (12.9 km) S Linden, along Yellow Poplar Trail
off US Hwy. 59, 56, 39, 12 November 2001 and 26 November 2002.
Dallas County, Cedar Hill State Park, DORBA and Talala Trails, 56,
49, 21 January and 16 November 2002. Morris County, Daingerfield
State Park, Dogwood Camping Area, 6 , 9, 26 November 2002. Taylor
County, Abilene State Park, Elm Creek Nature Trail, 46, 9, 17
November 2001. Titus County, Lake Bob Sandlin State Park, 36, 29,
juv., 21 December 2002.

Eurymerodesmus mundus is readily recognized by the large, hirsute,
clavate lobes on the caudal margin of the gonopodal aperture (Shelley
1990). Shelley speculated that the lobes must alter the millipeds’ posture
and locomotion because they are so disproportionately large in relation
to the rest of the body that they would otherwise scrape the substrate or
become impaled. The published record from Grayson County by
Shelley was inadvertently omitted from the text; its data are Grayson
County, Sherman, in storm cellar, 46, 79, 3 October 1967, M.
Cundliff (Florida State Collection of Arthropods, Gainesville). The sites
in Titus and Taylor counties are some 350 miles (563 km) apart, so E.
mundus thus occupies the entire breadth of the family’s distribution
across northern Texas. The species also inhabits a variety of biotopes
as habitats at these locales are quite different. The site in Cass County
is a climax forest on acreage owned by International Paper Company
that consists primarily of pines, yellow poplar and various oak species,
while the sites in Morris and Titus counties are within state parks and
comprised of mixed hardwoods. However, at the Dallas and Taylor
County sites, the dominant trees are live oak, mesquite and eastern red
cedar. In addition, the site in Dallas County includes trails situated near
native tall grass prairie habitat. Eurymerodesmus mundus ranges north¬
ward to Nebraska, and in the "Ark-La-Tex" region (Fig. 1). Its occur¬
rence in southwestern Arkansas (McAllister et al. 2002a) and north¬
eastern Texas near the Louisiana state line suggest potential discovery
in northwestern Louisiana (perhaps Bossier and/or Caddo parishes),
which would constitute a new state record. Interestingly, a large female

TEXAS J. SCI. 56(1), FEBRUARY, 2004

Figure 1 . Map of the United States with inset of Arkansas and parts of Louisiana, Oklahoma
and Texas showing county or parish distributions of Eurymerodesmus angularis (dots) and
E. mundus (stars) within these states. County distributions of E. mundus in Kansas and
Nebraska not included (see Shelley 1990).

Eurymerodesmus resembling E. mundus was collected by the senior
author on 6 January 2003 in the vicinity of Oil City, Caddo Parish;
however, an authentic male of E. mundus is necessary for specific
identification.

Specimens of E. angularis were also encountered in three counties in
the northeastern corner of Texas, confirming Shelley’s prediction (1990)
of discovery in this area. It represents a new species for Texas and the
tenth species of Eurymerodesmus in the state. Data are as follows:

Bowie Co., 5 mi (8 km) W Texarkana, along County Road 1217 off
FM 991, d , juv., 10 October 2001; S of Texarkana (Liberty Eylau) off
FM 558 along County Road 1370, lOd, 69, 11 October 2001 and 2d,
19 December 2001; Texarkana, Texas A&M University campus off
Robison Rd., 3d, 5 November 2001. Cass Co., Atlanta, Ellington
Clinic off U.S. Hwy. 59, 2d, 7 November 2002. Marion Co.,
Jefferson, 2997 FM 728, Cypress Bend Adventist Elementary School,
3d, 23 October 2002, and d, 4 mi (6.4 km) NW Jefferson, 9 November

THE TEXAS JOURNAL OF SCIENCE- VOL. 56, NO. 1, 2004

2002. All specimens above represent new county records.

Habitat at these sites is typical east Texas piney woods, and specimens
were encountered while moving along the ground after brief fall
showers. Eurymerodesmus angularis is a highly variable and widely
ranging species (Fig. 1), and the most proximate prior record to this
current study is that from the vicinity of Myrtis, ca. 30 miles (48.3 km)
NNW Shreveport, Caddo Parish, Louisiana (Shelley 1990). Despite
several efforts, no specimens of E. angularis were encountered in the
vicinity of Caddo Lake State Park in adjacent Harrison County, but its
presence is anticipated during the cooler and wetter months of fall and
winter. Shelley (1990) depicted four gonopodal variants of E. angularis
that he considered to be conspecific, and the northeast Texas form is that
found in Caddo Parish, with lightly sinuate gonopodal acropodites and
an aperture in which the caudolateral "pouch" flares strongly laterally.

To date little milliped sampling has taken place in northeast Texas
(Stewart 1969). In addition, northeast Texas likely forms the western
distribution boundary for a number of "eastern" diplopods and hence
justifies more intensive investigation. Recent studies in proximate parts
of Arkansas and Oklahoma produced several important discoveries
(McAllister et al. 2002a; 2002b; 2003a; 2003b; Shelley et al. 2003),
lending credence to this statement. Focused studies on the northeast
corner of Texas may be similarly profitable and are a primary objective
of future research.

Acknowledgments

The senior author thanks TAMU-T, particularly Drs. J. Johnson and
G. Mueller for providing Faculty Senate Research Enhancement Grants
nos. 140000 and 200900 to fund a portion of this study. We also thank
James T. McAllister, III (Brookhaven College, Dallas, Texas), and
Nancy Solley (TAMU-T) for assistance in collecting.

Literature Cited

McAllister, C. T., C. S. Harris, R. M. Shelley & J. T. McAllister, HI. 2002a. Millipeds
(Arthropoda: Diplopoda) of the Ark-La-Tex. I. New distributional and state records for
seven counties of the West Gulf Coastal Plain of Arkansas. J. Arkansas Acad. Sci.,
56:91-94.

McAllister, C. T., R. M. Shelley & J. T. McAllister, III. 2002b. Millipeds (Arthropoda:
Diplopoda) of the Ark-La-Tex. II. Distributional records for some species of western and
central Arkansas and eastern and southeastern Oklahoma. J. Arkansas Acad. Sci.,
56:95-98.

TEXAS J. SCI. 56(1), FEBRUARY, 2004

McAllister, C. T., R. M. Shelley & J. T. McAllister, III. 2003a. Millipeds (Arthropoda:
Diplopoda) of the Ark-La-Tex. III. Additional records from Arkansas. J. Arkansas
Acad. Sci., 57: (In press).

McAllister, C. T., R. M. Shelley & J. T. McAllister, III. 2003b. Millipeds (Arthropoda:
Diplopoda) of the Ark-La-Tex. IV. New geographic distribution records from
southcentral and southeastern Oklahoma. Proc. Oklahoma Acad. Sci., 83:(In press).
Shelley, R. M. 1990. Revision of the milliped family Eurymerodesmidae (Polydesmida:

Chelodesmidea) . Mem. Amer. Entomol. Soc., 37:1-112.

Shelley, R. M., C. T. McAllister & S. B. Smith. 2003. Discovery of the milliped
Pleuroloma flavipes Rafinesque in Texas, with a disjunct record from Louisiana, and new
localities from west of the Mississippi River (Polydesmida: Xystodesmidae). Entomol.
News 11 4: (In press).

Stewart, T. C. 1969. Records of millipeds in twenty five northeast Texas counties. Texas
J. Sci., 20(4): 383-385.

CTM at: chris.mcallister@tamut.edu
* * * * *

DIET OF THE WHITE-COLLARED SEEDEATER
SPOROPHILA TORQUEOLA (PASSERIFORMES: EMBERIZIDAE)

IN TEXAS

Jack C. Eitniear

Center for the Study of Tropical Birds, Inc. 218 Conway Drive
San Antonio, Texas 78209-1716

The white-collared seedeater (Sporophila torqueola), is a very small,
black and white finch about 11 cm in total length. The species has a
distribution from western Panama to the Rio Grande valley of Texas
(American Ornithologists’ Union 1998). Sporophila torqueola sharpei
occurs from the Rio Grande of Texas, south along the coastal plain of
northeastern Mexico to northern Veracruz, and west to eastern Nuevo
Leon and San Luis Potosi (American Ornithologists’ Union 1957). Most
papers on temperate subspecies of S. torqueola are taxonomic, with
virtually nothing written on its natural history, including diet (Eitniear
1997a). This paper summarizes dietary information collected in Texas
from 1995-2000.

White-collared seedeaters were studied at two sites in Zapata County,
Texas. Site 1 was located on the banks of the Rio Grande River within
the city of San Ygnacio (27°02’N 99°26’W) in a black willow ( Salix
niger) dominated community, with an understory of barnyardgrass
(Echinochloa crus-pavonis) , Louisiana cupgrass ( Eriochloa punctata),
spreading panicum {Panicum diffusum ), Bermudagrass ( Cynodon
dactylon) and Mexican sprangletop ( Leptochloa uninervia).

THE TEXAS JOURNAL OF SCIENCE— VOL. 56, NO. 1, 2004

Site 2, a marsh bordering a pond in Zapata County Park (26°54’N
099° 1 6’ W), was located within the city of Zapata. The habitat was
characterized by Bermudagrass, buffelgrass ( Cenchrus ciliaris ), Guinea-
grass ( Panicum maximum ), Johnson grass {Sorghum halepense), south¬
western bristlegrass {Setaria scheelei ), dock {Rumex chrysocarpus ) and
cattail {Typha domingensis) . Trees included sugar hackberry {Celtis
laevigata ), black willow, huisache {Acacia minuata) and guajillo {Acacia
berlandieri) . Plant identifications follow that of Hatch et al. (1990).

Methods and Materials

Observations were made from April to August 1995 at Site 1 (Eitniear
& Rueckle 1995) and August to October 1994, February 1996, April
1997 and April 2000 at Site 2. Observations began at either 0800 h or
1000 h and continued to about 1800 h or 1900 h. Five birds were
captured in mist- nets set at the site. Captured birds were leg banded and
placed in a holding cage until a fecal sample was caught on blotting
paper placed at the bottom of a small field cage. It was assumed these
bird’s fecal contents, although biased by a digestive differential of
certain foods, provided a representative sample of recently consumed
foods. The white uric acid covering was removed by flushing the
sample with water. The remaining fecal mass was stored in 70%
ethanol. Food items were identified by comparison to a reference
collection of seeds and leaves from all plants at the study sites (Smith
1970; Servat 1993). Observations of foraging birds were conducted
using 10 by 50 binoculars. Foraging observations were documented in
a field notebook and a botanical specimen, from plants that contained
seeds fed on, collected. Plant specimens were later identified by Robert
Lonard (UT-Pan American). On occasion seeds were obtained from the
mouths of captured birds. No effort, however, was made to flush crops.

Results and Discussion

Items in the diet of the species are summarized in Table 1. The
largest foraging group of seedeaters observed consisted of approximately
10 birds feeding on barnyardgrass and Louisiana cupgrass at Site 1.
The birds fed throughout the day, frequently retreating to nearby black
willows. Females were observed feeding Louisiana cupgrass seeds to
recently fledged young at this location (Eitniear & Rueckle 1995). Fecal
samples (five samples from five different birds) contained only barnyard
and Louisiana cupgrass seeds, thus supporting the theory that grasses
were the principle food resource consumed at this time. Green Louisi-

TEXAS J. SCI. 56(1), FEBRUARY, 2004

Table 1. Parts of 12 plants consumed by Sporophila torqueola sharpei in Zapata, Zapata
County, Texas, 1995-2000.

Plant Species

Part

Eriochloa cruz-pavornis

(seeds)

Panicum maximum*

(seeds)

Echinochloa punctata

(seeds)

Panicum diffiusum

(seeds)

Dichanthium annulafusum*

(seeds)

Panicum antidotale*

(seeds)

Cenchrus cilaris*

(seeds)

Setaria leucopila

(seeds)

Setaria scheelei

(seeds)

Acacia minuata

(floral parts)

Salix nigra

(floral parts)

Salix exigua

(floral parts)

*Non-native species

ana cupgrass seeds in the milky stage of development were collected
from the mouth and outer portions of the mandible of a female caught
in a mist net. Plant succession altered this site significantly during the
study. Black willow displaced barnyardgrass along the riverbank, and
plains bristlegrass, buffelgrass, Guineagrass and blue panicum became
established in open areas.

Seedeaters at Site 2 were observed feeding on southwestern bristle-
grass, barnyardgrass and Louisiana cupgrass. Bermudagrass, Guinea-
grass, Johnsongrass and buffelgrass also were abundant, and contained
ripe seeds, but not observed to be utilized as a food resource. Although
grass seeds dominated observations of white- collared seedeaters diet, at
1200 h on 25 February 1996 at Site 1, a male foraged on huisache
blossoms in a tree near the pond. For 30 minutes it was observed
consuming the orange globose clusters of stamens. Subsequent to this
observation, seedeaters had been observed feeding on the floral parts of
willow (Table 1).

Bill morphology of the genus Sporophila favors seed eating (Cody
1985). Observations made during this study, although somewhat
limited, support this concept. The greater proportion of barnyardgrass
in the diet of the white-collared seedeater may reflect the greater
abundance of this species over cupgrass and southwestern bristlegrass at
Site 2 (Eitniear 1997b). Despite barnyardgrass growing abundantly on
the opposite side of the pond at Site 2, seedeaters were never observed
feeding on it; perhaps because no cover existed nearby.

THE TEXAS JOURNAL OF SCIENCE- VOL. 56, NO. 1, 2004

Observations of feeding on the floral parts of willow and huisache in
addition to records of its feeding on berries in Costa Rica (Stiles &
Skutch 1989) and the pulp of Stemmadenia donnell-smithii in Mexico
(McMiarmid et al. 1977) indicates greater plasticity in diet than previous
authors have indicated (Cody 1985; Rubenstein et al. 1977). More
research is needed to determine dietary shifts in this species in relation
to changing seasons, variations in precipitation levels and landscapes.
Such research may indicate if the decline of this species from a formerly
robust widespread species in south Texas to the current patchily
distributed remnant population is principally the result of the use of
agrochemicals, habitat loss or some other factors (Eitniear & Rueckle
1996; Woodin et al. 1999).

Acknowledgments

I wish to thank the numerous field assistants that participated in this
study, especially Tom Rueckle. Robin Restall (Phelps Collection:
Venezuela), Dr. John T. Baccus (Texas State University), Dr. Robert
Lonard (University of Texas- Pan American), Dr. Keith Arnold (Texas
A&M University, College Station), Dr. Timothy Brush (Uni-versity of
Texas-Pan American) and Dr. Kent Rylander (Texas Tech University,
Junction) and two anonymous reviewers contributed valuable suggestions
to the study and/or manuscript. All birds were captured under permits
from the Texas Parks and Wildlife and the National Biological Survey.

Literature Cited

American Ornithologists’ Union. 1957. Check-list of North American Birds. The
American Ornithologists’ Union, Baltimore, Maryland, 691 pp.

American Ornithologists’ Union. 1998. Check-list of North American Birds. The
American Ornithologists’ Union, Washington D.C., 877 pp.

Cody, M. L. 1985. Habitat selection in birds. Academic Press, Inc., New York, 558 pp.
Eitniear, J. C. 1997a. White-collared Seedeater ( Sporophila torqueola ) in The Birds of
North America, No. 278 (A. Poole and F. Gill, eds). The Academy of Natural Sciences,
Philadelphia, PA, and The American Ornithologists’ Union, Washington, D.C., 12 pp.
Eitniear, J. C. 1997b. Diet and habitat preference of the White-collared Seedeater
(■ Sporophila torqueola sharpei ) in South Texas. Unpublished Master of Science Thesis,
Southwest Texas State University, 31 pp.

Eitniear, J. C. & T. Rueckle. 1995. Successful nesting of the White-collared Seedeater in
Zapata County, Texas. Bull. Tex. Ornithol. Soc., 28:20-22.

Eitniear, J. C. & T. Rueckle. 1996. Noteworthy avian breeding records from Zapata
County, Texas. Bull. Tex. Ornithol. Soc., 29:16-17.

Hatch, S. L., K. N. Gandi & L. E. Brown. 1990. Checklist of the vascular plants of
Texas. Tex. Agri. Exper. Station, College Station, Texas, 402 pp.

McDiarmid, R. W., R. E. Ricklefs & M. S. Foster. 1977. Dispersal of Stemmadenia
donnell-smithii ( Apocynaceae ) by birds, Biotropica 9:9-25.

TEXAS J. SCI. 56(1), FEBRUARY, 2004

Servat, G. 1993. A new method of preparation to identify arthropods from stomach
contents of birds. J. Field Ornithol., 64:49-54.

Smith, H. K. 1970. A method of analyzing fox squirrel stomach contents. Tech Series No.
3, Texas Parks and Wildlife Dept., 75 pp.

Stiles, G. F. & A. F. Skutch. 1989. A guide to the birds of Costa Rica. Cornell Univ.
Press, Ithaca, NY, 511 pp.

Woodin, M. C., M. K. Skoruppa, G. W. Blacklock & G. C. Hickman. 1999. Discovery
of a second population of white-collared seedeater, Sporophila torqueola
(Passeriformes : Emberizidae) along the Rio Grande of Texas. Southwest. Nat.,
44(4):535-538.

JCE at: JCE@cstbinc.org
*****

REPRODUCTION IN THE COFFEE SNAKE, N1NIA MACULATA
(SERPENTES: COLUBRIDAE), FROM COSTA RICA

Stephen R. Goldberg

Department of Biology, Whittier College
Whittier, California 90608

The coffee snake, Ninia maculata is known from Honduras, Nicara¬
gua, Costa Rica and Panama from 36-1800 m (Savage 2002). Fitch
(1970) reported N, maculata clutch sizes from Cartago Province, Costa
Rica. The purpose of this paper is to provide new information on the
reproductive cycle from a histological examination of gonads and
kidneys and additional data on clutch sizes.

A sample of 41 specimens of N. maculata from Costa Rica (females
n — 25, mean snout- vent length [SVL] = 226 mm ± 22 SD, range =
175-275 mm; males n = 16, SVL = 201 mm ± 15 SD, range = 179-
228 mm) was examined from the herpetology collection of the Natural
History Museum of Los Angeles County, Los Angeles (LACM). Snakes
were collected 1959-1996. Counts were made of enlarged ovarian
follicles (> 8 mm length) or oviductal eggs. The left testis, vas
deferens and a portion of the kidney were removed from males and the
left ovary was removed from females for histological examination.
Tissues were embedded in paraffin and sectioned at 5 /xm. Slides were
stained with Harris’ hematoxylin followed by eosin counterstain.
Histological slides were examined to determine the stage of the testicular
cycle and for the presence of yolk deposition (secondary vitellogenesis
sensu Aldridge 1979). Not all tissues were available for histological
examination due to damage or autolysis. Number of tissues histologi-

THE TEXAS JOURNAL OF SCIENCE- VOL. 56, NO. 1, 2004

Table 1 . Monthly distribution of stages in the ovarian cycle of Ninia maculata from Costa
Rica. Values shown are the numbers of females exhibiting each of the four conditions.

Month

Inactive

Early yolk
deposition

Enlarged follicles
> 12 mm length

Oviductal

eggs

February

June

July

August

September

October

November

Table 2. Clutch sizes for Ninia maculata (estimated from counts of yolked follicles > 8 mm
length or oviductal eggs*) from Costa Rica.

Date

SVL (mm)

Clutch size

Province

LACM #

11 February

240

Cartago

153798

29 June

230

Limon

153808

11 July

215

Cartago

153828

2-6 August

220

Guanacaste

153788

27 August

210

San Jose

153857

30 August

220

San Jose

153843

15 September

225

San Jose

153851

16 September

246

Cartago

153802

13 October

213

San Jose

153831

10 November

190

San Jose

153849

14 November

225

San Jose

153856

20 November

223

San Jose

153823

20 November

240

San Jose

153821

22 November

233

San Jose

153835

cally examined by specimen were: testis = 16, vas deferens = 3, kidney =
1 3 , ovary = 11. Follicles in advanced stages of yolk deposition or oviductal
eggs were counted, but were not examined histologically. An unpaired Mest
was used to compare body sizes of male and female samples. The relationship
between female SVL and clutch size was examined by linear regression
analysis.

Material examined — The following specimens of Ninia maculata were
examined by Costa Rica province: CARTAGO (LACM 153787, 153795,
153798, 153799, 153801-153805, 153828), GUANACASTE (LACM
153788, 153789), LIMON (LACM 153807, 153808, 153812),

PUNTARENAS (LACM 153790), SAN JOSE (LACM 38063, 38064,
153818, 153819, 153821, 153823, 153824, 153826, 153829, 153831,
153834, 153835, 153839, 153840, 153843, 153844, 153846,

153848-153852, 153856-153858).

Testicular histology of N. maculata was similar to that reported by
Goldberg & Parker (1975) for two colubrid snakes, Masticophis

TEXAS J. SCI. 56(1), FEBRUARY, 2004

Figure 1 . Linear regression of female body size (mm) versus clutch size for fourteen Ninia
maculata from Costa Rica.

taeniatus and Pituophis catenifer. All testes examined exhibited
spermiogenesis with metamorphosing spermatids and sperm present.
The following numbers of males were undergoing spermiogenesis by
month: February (3), April (1), June (3), July (2), August (2),
September (1), October (2), November (2). All three vasa deferentia
examined contained sperm: April (1), July (1), November (1). All
thirteen kidney sexual segments examined were enlarged and contained
secretory granules: February (2), April (1), June (2), July (2), August
(1), September (1), October (2), November (2). Mating usually
coincides with enlargement of the kidney sexual segments (Saint Girons
1982). The smallest spermiogenic males measured 179 mm SVL
(LACM 153805, 153858). Males smaller than this size were not
examined, therefore the minimum size at which N. maculata begins
sperm formation is unknown.

Females were significantly larger than males (unpaired f-test, t =
4.01, df = 39, P < 0.001). Females with enlarged follicles (> 8 mm
length) or oviductal eggs were observed February, June-November
(Table 1). The smallest reproductively active N. maculata female (one
oviductal egg) measured 190 mm SVL (Table 2), while the three females
undergoing early yolk deposition measured 207 mm SVL (14 November,

THE TEXAS JOURNAL OF SCIENCE- VOL. 56, NO. 1, 2004

LACM 153818), 240 mm SVL (27 August, LACM 153850), 246 mm SVL
(22 November, LACM 153852). The minimum size at which N.
maculata females commence reproduction remains to be determined.
There was no evidence that females produce more than one clutch of
eggs in a reproductive season (i.e., oviductal eggs and yolk deposition
in progress in the same female) although the presence of reproductively
active females during seven months of the year (Table 2) suggests this
might be possible. Fitch (1970) reported gravid female N. maculata
from Volcan Turrialba, Cartago Province, Costa Rica that measured 187,
206, 218, 222, 231 and 233 mm SVL respectively. A dissected female
contained five eggs. One female was collected 2 June and three were
collected 30 August.

All clutch sizes are listed in Table 2. Mean clutch size for 14 egg
clutches from Costa Rica was 2.9 ± 1.1 SD, range = 1-5. Linear
regression analysis revealed a significant positive correlation between
female body size and clutch size Y = -9.87 -I- 0.06X, r = 0.77, P =
0.001 (Fig. 1).

The preceding observations on the ovarian cycle and the presence of
males undergoing spermiogenesis during eight months of the year
suggests that N. maculata has a prolonged reproductive cycle. Fitch
(1970) similarly concluded that N. maculata reproduced throughout
much of the year in Costa Rica, if not all of it.

Acknowledgments

I thank D. A. Kizirian (LACM) for permission to examine specimens,
K. R. Beaman (LACM) for his comments and P. Firth for Fig. 1.

Literature Cited

Aldridge, R. D. 1979. Female reproductive cycles of the snakes Arizona elegans and
Crotalus viridis. Herpetologica, 35(3):256-261.

Fitch, H. S. 1970. Reproductive cycles in lizards and snakes. Univ. Kansas, Mus. Nat.
Hist., Misc. Publ., 52:1-247.

Goldberg, S. R. & W. S. Parker. 1975. Seasonal testicular histology of the colubrid
snakes, Masticophis taeniatus and Pituophis melanoleucus . Herpetologica,
31(3):317-322.

Saint Girons, H. 1982. Reproductive cycles of male snakes and their relationships with
climate and female reproductive cycles. Herpetologica, 1 8(3) :5- 16.

Savage, J. M. 2002. The amphibians and reptiles of Costa Rica: A herpetofauna between
two continents, between two seas. University of Chicago Press, Chicago, Illinois, 934

pp.

SRG at: sgoldberg@whittier.edu

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Jones, T. L. 1971. Vegetational patterns in the Guadalupe Mountains,
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Smith, J. D. 1973. Geographic variation in the Seminole bat, Lasiurus
seminolus J. Mammal., 54(l):25-38.

Smith, J. D., & G. L. Davis. 1985. Bats of the Yucatan Peninsula.
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Jones, T. L. 1975. An introduction to the study of plants. John Wiley
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Davis, G. L. 1975. The mammals of the Mexican state of Yucatan.
Unpublished Ph.D. dissertation, Texas Tech Univ. , Lubbock, 396 pp.

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THE TEXAS JOURNAL OF SCIENCE- VOL. 56, NO. 1, 2004

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DIRECTORS

2001 David S. Marsh, Angelo State University

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THE TEXAS JOURNAL OF SCIENCE

Volume 56, No. 2

May, 2004

CONTENTS

Natural Source of Arsenic in East Texas Lake Sediments.

By Kathy Judy, E. B . Ledger and C. A. Barker . 91

Community Ecology of Freshwater, Brackish and Salt Marshes of the
Rio Grande Delta.

By Frank W. Judd and Robert /. Lonard . 103

Physiological Tolerance Ranges of Larval Caenis latipennis (Ephemeroptera:

Caenidae) in Response to Fluctuations in Dissolved Oxygen Concentration,
pH and Temperature.

By Robert T. Puckett and Jerry L. Cook . 123

Natural History of the Southern Plains Woodrat Neotoma micropus (Rodentia:

Muridae) from Southern Texas.

By John R. Suchecki, Donald C. Ruthven, Ill, Charles F. Fulhorst

and Robert D. Bradley . 131

Adult Foraging Behavior in Meams’ Grasshopper Mouse, Onychomys arenicola
(Rodentia: Muridae) is Influenced by Early Olfactory Experience.

By Fred Punzo . 141

Robotics Repeatability and Accuracy: Another Approach.

By Jan Brink, Bill Hinds and Alan Haney . 149

Historical Population Dynamics of Red Snapper ( Lutjanus campechanus) in the
Northern Gulf of Mexico.

By J. R. Gold and C. P. Burridge . 157

General Notes

Notes on Reproduction in the False Coral Snakes, Erythrolamprus bizona

and Erythrolamprus mimus (Serpentes: Colubridae) from Costa Rica.

By Stephen R. Goldberg . 171

A New Distribution Record and Notes on the Biology of the Brittle Star
Ophiactis simplex (Echinodermata: Ophiuroidea) in Texas.

By Ana Beardsley Christensen . 175

First Definitive Record of more than Two Nesting Attempts by Wild
White- winged Doves in a Single Breeding Season.

By Cynthia L. Schaefer, Michael F. Small, John T. Baccus

and Roy D. Welch . 179

Annual Meeting Notice for 2005 . . . . 183

Membership Application . 184

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Associate Editor for Chemistry:

John R. Villarreal, The University of Texas-Pan American
Associate Editor for Computer Science:

Nelson Passos, Midwestern State University
Associate Editor for Environmental Science:

Thomas LaPoint, University of North Texas
Associate Editor for Geology:

Ernest L. Lundelius, University of Texas at Austin
Associate Editor for Mathematics and Statistics:

E. Donice McCune, Stephen F. Austin State University
Associate Editor for Physics:

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AFFILIATED ORGANIZATIONS
American Association for the Advancement of Science,

TEXAS J. SCI. 56(2):91-102

MAY, 2004

NATURAL SOURCE OF ARSENIC
IN EAST TEXAS LAKE SEDIMENTS

Kathy Judy*, E. B. Ledger and C. A. Barker

* Department of Geology, Blinn College
Bryan, Texas 77805 and

Department of Geology, Stephen F. Austin State University
Nacogdoches , Texas 75962

Abstract.— Elevated arsenic levels occur in the sediment of several east Texas reservoirs.
Eight reservoirs exceed the statewide 85th percentile of 17 mg/kg dry weight for arsenic in
lake sediment. Average arsenic concentrations in the sediments of these lakes ranges from
19.5-83.5 mg/kg. The source of the arsenic is the marine mudstone formations which crop
out in east Texas. Arsenic is common in marine mudstone where it substitutes for sulfur in
the mineral pyrite. Unusually high levels of arsenic (up to 122 mg/kg compared to a global
average of 13 rag/kg) are known to occur in the Weches Formation in east Texas. Other east
Texas marine mudstone formations have not been analyzed for arsenic content. Oxidation
of arsenic-bearing pyrite produces acid sulfate conditions, precipitated Fe(OH)3 and oxidized
arsenic species. Arsenic species readily adsorb to Fe(OH)3 which is transported to reservoirs
by streams and incorporated into the sediment.

Arsenic has recently been found to occur at elevated levels in some
east Texas rock units (Ledger & Judy 2003). It probably substitutes for
sulfur in the ubiquitous mineral pyrite. Pyrite occurs in a variety of
geologic settings, including marine mudstone formations in which iron
and sulfur were both present and conditions were sufficiently anaerobic
to reduce them. This type of depositional environment was present at
times in east Texas during the Eocene. Present day exposure of py rite¬
bearing mudstone formations to oxygenated surface and ground water
oxidizes the pyrite and releases arsenic into the environment. Monitor¬
ing of streams and lakes by the Texas Commission on Environmental
Quality (TCEQ) generally shows levels of arsenic in lake water well
below the MCL (Maximum Contaminant Level) established by the EPA.
However, elevated arsenic levels occur in the sediment of several east
Texas reservoirs.

Geologic Setting

The Claiborne Group consists of a thick series of cyclic transgressive/
regressive sedimentary strata deposited in east Texas during the middle
Eocene (Deussen 1911; Dumble 1918; Berg 1970; Collins 1980; Collins
1982). The Queen City Sand, Sparta Sand, Carrizo Sand and Yegua
Formations are composed of fine to medium grained sand deposited in

THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 2, 2004

a nearshore environment. The Reklaw Formation, Weches Formation
and Cook Mountain Formation are composed primarily of mudstone
deposited in a quiet marine environment such as a lagoon or shelf
(Figure 1).

There are few data available, but the pyrite content of the mudstone
formations appears to vary laterally and can be appreciable. Selected
hand specimens from the southern part of the Weches Formation contain
as much as 10% pyrite with some crystals being up to a few millimeters
in diameter. Further north, pyrite is rare, while siderite (FeC03) is
abundant.

The arsenic content is virtually unknown, but likely to be high where
pyrite is abundant. Eight samples from a road cut near Nacogdoches,
Texas average almost 100 mg/kg arsenic (Ledger & Judy 2003) com¬
pared to a global average shale value of 13 mg/kg.

Present day weathering of the mudstones occurs most rapidly where
the formations crop out or are near the surface. This process releases
soluble arsenic oxides into ground and surface water. Past structural
events have affected the outcrop patterns, stream patterns, and even the
deposition of east Texas rock units. Most of the rock layers in the
eastern half of Texas dip gently to the southeast, toward the Gulf of
Mexico. However, the dip rate flattens out and then reverses to north¬
west or west dip on the Texas side of the Sabine Uplift, a circular
regional structure located in northeast Texas and northwest Louisiana
over a basement high (Nicolas & Waddell 1989). An uplift is an area
where deep rocks have been pushed upward. The zone of flat to re¬
versed dip on the flank of the Sabine Uplift causes the Weches, and
other possibly arsenic bearing formations, to have a much wider outcrop
area than they would have otherwise. Jackson & Laubach (1991) con¬
cluded that the Sabine area was uplifted about 170m during the middle
of the Cretaceous, and that a second episode of uplift occurred early in
the Eocene.

Three major fault systems also affect east Texas rock outcrops: the
Mt. Enterprise, Mexia and Talco fault zones. These fault systems
consist of down-dropped grabens bounded by normal faults which
formed when overloading of sedimentary rock deposits above the
unstable low-density Louann Salt caused the salt to flow and intrude
upward into areas of lesser pressure (Jackson & Wilson 1982). The Mt.

JUDY, LEDGER & BARKER

Figure 1. Stratigraphic column of the Middle Eocene Claiborne Group of east Texas
(modified from Satin & Brooks 1977).

Enterprise fault system is a linear zone of grabens trending east north¬
east that are bounded by growth faults that were active during the time
of sediment deposition (Ferguson 1984). Structural control of stream
drainage patterns shows up on detailed maps as stream segments aligned
with faults and grabens (Baumgardner 1987). Fault and joint fracture
planes are primary conduits for movement of ground water through
otherwise impermeable mudstone layers and thus may exert significant
control on the localization of arsenic, iron and other elements.

Results of Weathering

Oxidation of pyrite produces Fe(III) and acid sulfate conditions.
Fe(III) is mobile below about pH 3-4. At higher pH, Fe(III) quickly
hydrolyzes to precipitate as amorphous Fe(OH)3, a red, colloidal gel.

THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 2, 2004

This is easily transported by streams as suspended or bed load and
settles out in calmer lake settings.

Initial breakdown of pyrite underground:

2FeS2 + 2H20 + 702 = > 2Fe2+ + 4S042 + 4H+

Oxidation and hydrolysis of Fe2+ in contact with atmosphere:

4Fe2+ + 02 + 10H2O = > 4Fe(OH)3 + 8H+

Under strong oxidizing conditions, As(V) is thermodynamically
stable, but the As(III)/As(V) transformation occurs at such a slow rate
that both species are usually present. H2As03 and H2As04' are the most
abundant species in well oxygenated surface water between pH 3-7.
Arsenic species readily adsorb to Fe-oxides and clay minerals and
become incorporated in the sediment of streams and lakes.

Rates of Weathering

The rate at which pyrite oxidizes in natural environmental systems is
usually accelerated by the action of sulfur and iron oxidizing bacteria
such as Thiobacillus sp. , Ferrobacillus sp. , Gallionella , Sphaerotilus and
others (Langmuir 1997). Rates of oxidation caused by bacterial catalysis
vary greatly depending on pH, surface area of pyrite, dissolved oxygen
concentration and other factors. However, the rate increase is com¬
monly in orders of magnitude (Olson 1991; Stumm & Morgan 1996;
Edwards et. al. 1998).

Such rapid oxidation results in pH levels low enough that Fe(OH)3
does not form and arsenic species are mobile in ground or surface
waters. Judy (1999) measured pH as low as 3.95 in distilled water
mixed with dried samples of the Reklaw formation.

Screening Levels for Arsenic

Currently, no federal or state standards for allowable levels of arsenic
in lake sediments exist. The National Oceanic and Atmospheric Admin¬
istration (NOAA 1999) has established probable effects levels (PELs) for
substances at which they are likely to be toxic. For arsenic in lake
sediment, the PEL is 32.7 mg/kg. To identify water bodies with ele¬
vated sediment metals concentrations, the TCEQ uses a statewide 85th
percentile. These are derived from long-term monitoring data and
indicate concentrations below which 85 % of measurements occur. State-

JUDY, LEDGER & BARKER

Table 1 . Average concentration of arsenic in sediment (mg/kg) for twenty-one lakes in east
Texas (data provided by the TCEQ, 1985-003).

Reservoir

Average Concentration
of Arsenic in Sediment
(mg/kg)

Number

Samples

Lake Nacogdoches

83.5

Lake Jacksonville

53.8

Sam Rayburn Reservoir

34.1

Lake Cherokee

31.0

Ellison Creek Reservoir

30.3

Pinkston Reservoir

28.0

Lake Tyler East

24.1

Lake Tyler

20.0

Lake Palestine

10.3

Lake O’ the Pines

8.9

Martin Lake

8.8

Caddo Lake

8.7

Wright Patman Lake

6.1

Lake Monticello

5.8

Houston County Lake

5.8

Lake Bob Sandlin

5.3

Lake Cypress Springs

4.2

Toledo Bend Reservoir

3.3

Lake Fork Reservoir

2.7

Lake Murvaul

2.5

Lake Tawakoni

1.7

wide 85th percentiles indicate areas where metals concentrations are
elevated and are not based on negative biological effects. For arsenic
in sediment in reservoirs, the statewide 85th percentile is 17 mg/kg,
close to the global average of 13 ppm for shale.

Methods

All data for arsenic levels in lake sediments were provided by the
Texas Commission on Environmental Quality (TCEQ) and are available
to the public. If available, data collected between 1 January 2000 and
1 April 2003 were used. Some lakes were not monitored for arsenic in
sediment during this time period. For these, data acquired between
1985 and 2000 were used.

Surface outcrops of the Weches Formation, Reklaw Formation and
Cook Mountain Formation are those shown on the Geologic Atlas of
Texas Texarkana Sheet (Barnes 1979), Palestine Sheet (Barnes 1993)
and Tyler Sheet (Barnes 1975). Stream drainage patterns were illus¬
trated based on the Geologic Atlas of Texas and USGS topographic
maps.

THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 2, 2004

Results and Discussion

In general, lakes receiving substantial discharge from streams flowing
through mudstone formations have elevated levels of arsenic in their
sediments. Eight of the twenty-one lakes for which arsenic in sediment
data are available exceed the statewide 85th percentile of 17 mg/kg and
three exceed the PEL of 32.7 mg/kg (Table 1). Four of these: Lake
Nacogdoches (Figure 2), Lake Jacksonville (Figure 3), Lake Tyler
(Figure 4) and Ellison Creek Reservoir (Figure 5) are near outcrops of
the Weches Formation and are fed by streams which flow through it.
Lake Cherokee (Figure 6) is fed by discharge from streams flowing
through outcrops of the Reklaw Formation which may contain elevated
arsenic levels. Sam Rayburn Reservoir (Figure 7) is fed by large
streams which flow across the Weches, Reklaw and Cook Mountain
Formations. Lake Tyler East (Figure 4) and Pinkston Reservoir have
elevated sediment arsenic levels but do not have a source that is apparent
on the geologic map.

The remaining thirteen lakes are all well below the statewide 85th
percentile. Ten of these are fed by streams which flow primarily across
sand formations. The remaining three: Lake Palestine (Figure 8); Lake
O’ the Pines (Figure 5); and Houston County Lake receive some stream
drainage from mudstone outcrops, but do not show elevated levels of
arsenic in their sediment.

Individual study of the Eve lakes which appear to be anomalous is
likely to reveal a simple explanation for the levels of arsenic present.
For example, Lake O’ the Pines (Figure 5) is near the northern Weches
in which siderite formed and pyrite is rare. Field research by the
authors found that surface outcrops in this area are very thin, only a few
feet in some locations. Also, small reservoirs are present on the two
major streams flowing across the Weches Formation into Lake O’ the
Pines. These would trap sediment before it gets to the lake. Therefore,
it is seems that arsenic is either not present, not abundant, or is being
trapped in the smaller reservoirs.

The proximity of a reservoir to mudstone outcrops is not a perfect
predictor of elevated arsenic levels in lake sediments. However, the
correlation observed here suggests that this would be useful in deciding
which lakes to most closely monitor.

JUDY, LEDGER & BARKER

Miles

Ew Weches
Formation

Figure 2. Lake Nacogdoches, Texas. Arsenic-bearing formation outcrop is shown in dark
gray. Arrow with number indicates average concentration of arsenic in sediments in
mg/kg dry weight at sampling sites.

Figure 3. Lake Jacksonville, Texas. Arsenic-bearing formation outcrop is shown in dark
gray. Arrows with numbers indicate average concentrations of arsenic in sediments in
mg/kg dry weight at sampling sites.

THE TEXAS JOURNAL OF SCIENCE- VOL. 56, NO. 2, 2004

Evv Weches Formation

Figure 4. Lake Tyler and Lake Tyler East, Texas. Arsenic-bearing formation outcrop is
shown in dark gray. Arrows with numbers indicate average concentrations of arsenic in
sediments in mg/kg dry weight at sampling sites.

Figure 5. Ellison Creek Reservoir and Lake O’ the Pines, Texas. Arsenic-bearing formation
outcrop is shown in dark gray. Arrows with numbers indicate average concentrations of
arsenic in sediments in mg/kg dry weight at sampling sites.

JUDY, LEDGER & BARKER

Er Reklaw Formation

Figure 6. Lake Cherokee, Texas. Arsenic-bearing formation outcrop is shown in dark gray.
Arrows with numbers indicate average concentrations of arsenic in sediments in mg/kg
dry weight at sampling sites.

Figure 7. Sam Rayburn Reservoir, Texas. Arsenic-bearing formation outcrop is shown in
dark gray. Arrows with numbers indicate average concentrations of arsenic in sediments
in mg/kg dry weight at sampling sites.

100

THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 2, 2004

Figure 8. Lake Palestine, Texas. Arsenic-bearing formation outcrop is shown in dark gray.
Arrows with numbers indicate average concentrations of arsenic in sediments in mg/kg
dry weight at sampling sites.

Arsenic in lake sediments is not bioavailable to pelagic organisms or
organisms that drink the lake water. Its possible effects on benthic
organisms may be a field of future study. An interesting and un¬
answered question is whether or not arsenic is bioavailable at any time
between the initial weathering of arsenic-bearing pyrite and the deposi¬
tion of Fe(OH)3 with adsorbed arsenic species.

JUDY, LEDGER & BARKER

101

Acknowledgments

We thank Ken Farrish and Chris Mathewson for comments on an
earlier draft of the manuscript. We thank the TCEQ for their very well
organized system for managing information and making it available to
the public.

Literature Cited

Barnes, V. E. 1993. Geologic atlas of Texas: Palestine Sheet. Austin, Texas, Bureau of
Economic Geology, The University of Texas at Austin, 1:250 000, 1 sheet.

Barnes, V. E. 1979. Geologic atlas of Texas: Texarkana Sheet. Austin, Texas, Bureau of
Economic Geology, The University of Texas at Austin, 1:250 000, 1 sheet.

Barnes, V. E. 1975. Geologic atlas of Texas: Tyler Sheet. Austin, Texas, Bureau of
Economic Geology, The University of Texas at Austin, 1:250 000, 1 sheet.
Baumgardner, R. W., Jr. 1987. Landsat-based lineament analysis, east Texas basin and
Sabine Uplift area. The University of Texas at Austin, Bureau of Economic Geology,
167:1-26.

Berg, R. R. 1970. Outcrops of the Claiborne Group in the Brazos Valley, Southeast Texas.

Guidebook, Texas A&M Univ. Dept, of Geology, College Station, 54 pp.

Collins, A. M. 1982. Petrology of the Eocene Marquez Shale Member of the Reklaw
Formation, Bastrop County, Texas. Unpublished M.S. Thesis, The Univ. of Texas,
Austin, 142 pp.

Collins, E. W. 1980. The Reklaw Formation of east Texas. Pp. 67-70, in Middle Eocene
coastal and nearshore deposits of east Texas, a field guide to the Queen City Formation
and related papers (B.F. Perkins, and D.K. Hobday, eds.), SEPM, Tulsa, Oklahoma, 95

pp.

Deussen, A. 1911. Notes on some clay from Texas. US Geological Survey Bulletin,
470:302-351.

Dumble, E. T. 1918. The geology of east Texas. University of Texas Bulletin, 1869, 388

pp.

Edwards, K. J., M. O. Schrenk, R. Hamers & J. Banfield. 1998. Microbial oxidation of
pyrite: Experiments using microorganisms from an extreme acidic environment. Am.
Min., 83:1444-1453.

Ferguson, J. D. 1984. Jurassic age salt tectonism within the Mt. Enterprise Fault System,
Rusk County, Texas. Pp. 157-161, in The Jurassic of East Texas (M. W. Presley, ed.),
East Texas Geological Society, 304 pp.

Jackson, M. L. W. & S. E. Laubach. 1991. Structural history and origin of the Sabine
arch, east Texas and northwest Louisiana. The University of Texas at Austin, Bureau of
Economic Geology, Geological Circular, 91-3:1-47.

Jackson, M. P. A. & B. D. Wilson. 1982. Fault tectonics of the east Texas basin. The
University of Texas at Austin, Bureau of Economic Geology, 31 pp.

Judy, K. 1999. Clay mineralogy and electrical conductivity of the Claiborne Group,
Eastern Texas. Unpublished M.S. Thesis, Stephen F. Austin State Univ., Nacogdoches,
124 pp.

Langmuir, D. 1997. Aqueous environmental geochemistry. Prentice Hall, New Jersey,
vii-f 600 pp.

Ledger, E. B. & K. Judy. 2003. Elevated arsenic levels in the Weches Formation,
Nacogdoches County, Texas, GSAGS Transactions, in press.

Nicolas, R. L., & D. E. Waddell. 1989. The Ouachita system in the subsurface of Texas,

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Arkansas, and Louisiana. Pp. 661-672 in The Geology of North America, Vol. F-2, The
Appalachian-Ouachita Orogen in the United States (R.D. Hatcher, Jr. , W. A. Thomas, and
G.W. Viele, eds.), Geological Soci ety of America, xiii-t-767 pp.

NOAA. 1999. NOAA Screening Quick Reference Tables (SquiRTs). NOAA, Seattle,
Washington.

Olson, G. J. 1991. Rate of pyrite bioleaching by Thiobacillus ferrooxidans : Results of an
interlaboratory comparison. Applied and Environmental Microbiology, 57:642-644.

Sartin, A. A. & E. C. Brooks. 1977. Heavy mineral analysis of Queen City and Sparta
Formations (Eocene) in east Texas, The Compass of Sigma Gamma Epsilon, 54:72-77

Stumm, W. & J. J. Morgan. 1996. Aquatic Chemistry 3d ed. Wiley-Interscience, New
York, xvi + 1022 pp.

EBL at: eledger@sfasu.edu

TEXAS J. SCI. 56(2): 103-122

MAY, 2004

COMMUNITY ECOLOGY OF FRESHWATER,

BRACKISH AND SALT MARSHES OF
THE RIO GRANDE DELTA

Frank W. Judd and Robert I. Lonard

Department of Biology
University of Texas-Pan American
Edinburg, Texas 78541-2999

Abstract.-— Species composition and importance, species diversity and evenness, species
richness, and community similarity are compared among 6 freshwater, 9 brackish and 1 1 salt
marshes in the Rio Grande Delta. Community similarity is generally low among marshes,
but salt marshes have a greater mean coefficient of similarity than brackish marshes. Species
richness per marsh ranges from 15 to 31 for freshwater marshes, 7 to 24 for brackish
marshes and 7 to 26 for salt marshes. Each freshwater marsh has a different dominant
species. The first six species in importance in all three kinds of marshes contribute from
72.6 to 99.8% of the relative cover. Thus, most species are of low importance. There is
no significant difference in species richness, species diversity or evenness among the three
kinds of marshes. The generalization of the relationships found in this study awaits
additional information on marshes from other areas of the Texas coast.

The physiography of southern Texas is characterized by offshore
barrier islands, an enclosed lagoon (Laguna Madre), and the delta of the
Rio Grande on the Texas mainland. The base of the delta is about 46
km long extending from Port Mansfield in Willacy County to the mouth
of the Rio Grande in Cameron County. The apex of the delta is located
approximately 66 km inland from the Gulf of Mexico (Brown et al.
1980).

Prior to the construction of dams, floodways and levees, the Rio
Grande overflowed its banks annually depositing new sediment and
moving water into a variety of meander channels in the delta. These
flood waters constituted significant freshwater input into the wetlands of
the Rio Grande Delta. However, in the past 50 years dams and flood
control projects have eliminated this source of freshwater (Jahrsdoerfer
& Leslie 1988) and the wetlands are now dependent on rainfall alone for
freshwater input.

Unlike streams of the upper and central Texas coast, the Rio Grande
does not have associated swamps or freshwater marshes (White et al.
1986). Rather, there is a gradational array of infrequently to permanent¬
ly inundated wetlands in the Rio Grande Delta. Brackish marshes are
common because: (1) evaporation exceeds precipitation, (2) prevailing
southeasterly winds carry salt spray inland from the Laguna Madre and,
(3) extremely high storm tides flow inland along drainage courses during

104

THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 2, 2004

hurricanes (Brown et al. 1980). Salt marshes are less common and less
extensive because wind-tidal flats occupy the areas of the delta that are
typically occupied by salt marshes on the central and upper Texas Coast
(Brown et al. 1980). Freshwater marshes are even more uncommon
because of the absence of freshwater input by river overflow and low
annual rainfall.

Little information is available on the marshes of the Rio Grande
Delta. White et al. (1986) used color- infrared photographs to identify
and classify wetlands in the delta. They recognized seven major kinds
of wetlands including freshwater, brackish and salt marshes. Kinds of
marshes were distinguished based on elevation, vegetation and soil and
surface moisture. Lists of species characteristic of each type of marsh
were provided, but many of the species used to characterize the vegeta¬
tion of a given kind of marsh were also listed as characteristic of one or
both of the other types of marsh. There was no quantification of species
abundance or diversity.

Johnston (1955) recognized differing marsh communities along an
elevation gradient. He reported that at low elevations a community
comprised of Bat is maritima , Salicomia virginica and Suaeda linearis
graded almost imperceptibly into slightly higher elevations characterized
by Borrichia frutescens, B. maritima and Monanthochloe littoralis,
which in turn graded into a community of Spartina spartinae. Judd et
al. (1997a) used multispectral videography to distinguish the pattern of
zonation and species composition in a brackish marsh at Laguna
Atascosa National Wildlife Refuge (LANWR), Cameron County, Texas.
At the lowest elevations there was a distinct zone dominated by maritime
saltwort, B. maritima. Intermediate elevations supported a zone
dominated by shoregrass, M. littoralis. At the highest elevations the
third zone was dominated by Gulf cordgrass, S. spartinae. The upper
margin of this zone graded into a shrub-grassland community that
occurred on lomas (clay dunes). A salt marsh also was organized into
three zones along an elevation gradient and had the same dominant
species in each zone (Judd et al. 1997b). Judd & Lonard (2002)
compared species richness and diversity in a brackish and salt marsh at
LANWR. Forty-seven species were present in the two marshes, but
only 15 were common to both. Monanthochloe littoralis and B.
maritima were the dominant species in the brackish marsh and S .
spartinae was dominant in the salt marsh. In both marshes, four species
contributed from 73% to 86% of the cover. Consequently, most species
contributed little to vegetation abundance and community structure.
There were no significant differences in species diversity within marshes

JUDD & LONARD

105

between years or between marshes within a year.

Lonard & Judd (1999) catalogued the vascular plant species found in
fresh, brackish and salt marshes in the Rio Grande Delta based on a
survey of 27 marshes. They found 84 species representing 27 families
were present. Thirty-five species were limited to freshwater marshes
and 12 species were limited to salt marshes. No species were unique to
brackish marshes. Occurrence in fresh, brackish and salt marshes was
provided for each species, but there was no quantification of abundance
or comparison of species richness or community similarity among the
kinds of marshes.

Marshes of the Rio Grande Delta provide critical habitat for numerous
waterfowl species and several threatened and endangered mammalian
species. It is important to know the composition, structure, species
diversity and fidelity of marsh communities in the Rio Grande Delta to
facilitate re-establishment of native vegetation at disturbed sites and to
facilitate wise management decisions relative to providing appropriate
habitat for marsh fauna. To date, quantified information on species
abundance, diversity and community similarity are available for only one
brackish and one salt marsh in the Rio Grande Delta. Herein, this study
reports on the species composition, species diversity and species richness
of 6 freshwater, 9 brackish and 1 1 salt marshes in the Rio Grande Delta.
Community similarity, dominant species, species richness, species
diversity and evenness are compared among these marshes.

Materials and Methods

The locations of marshes studied are given in Table 1. The line
intercept method (Canfield 1941) was used to quantify species abun¬
dance. The number of transects sampled at each site was dependent
upon the size and configuration of the wetland basin. A minimum of
two and a maximum of 10 transects were sampled at the marshes.
Transects were established along an elevation gradient extending from
the low point in the marsh until an interval with upland vegetation (trees
and shrubs) was encountered. Each transect was divided into 10 m
intervals and readings were taken along the length of each interval.
Each species intercepted by the line was rated individually and was
recorded without separation into strata (i.e., tree, shrub and ground
layers). Species and foliage cover were recorded and from these data
the frequency of occurrence, relative frequency, relative cover and an
importance value which is the sum of relative frequency and relative
cover were calculated. The importance value was used to determine
dominant species.

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THE TEXAS JOURNAL OF SCIENCE— VOL. 56, NO. 2, 2004

Table 1. Marshes studied, their locations and mean salinities. NWR = National Wildlife
Refuge, TPWD = Texas Parks and Wildlife Department. LANWR = Laguna Atascosa
National Wildlife Refuge, NPS = National Park Service.

Marsh

Location

Mean Salinity

Freshwater Marshes

Paso Real, TPWD

26° 18’55.56"

97°31’27.48" W

0.5

Russelltown

26°04’51 .25"

97°34’52.50" W

0.5

Resaca de la Palma, TPWD

25°58’32.86"

97°34’00.76" W

0.0

Audubon Sabal Palm Sanctuary

25”5r00.76"

97°25’07. 15" W

0.0

Cattail Lake, Santa Ana NWR

26°04’32.41"

98°09’14. 15" W

0.0

Willow Lake, Santa Ana NWR

26°05’00.72"

98°08’ 18.79" W

0.5

Brackish Marshes

Palo Alto #1, NPS

26°0ri7.43"

97°28’ 12.26" W

6.0

Palo Alto #2, NPS

26°00’ 18.04"

97°27’18.55" W

6.0

Laguna Atascosa NWR Resaca

26° 10’21 .00"

97° 19’53.55" W

17.0

Olmito Resaca

26°00’48.75"

97°32’30.14" W

2.3

Tio Cano #1, NWR

26°12’37.01"

97°48’50.43 " W

4.5

Tio Cano #2, NWR

26° 12’39.36"

97°48’47.82" W

3.8

Bay view Resaca #1

26°07’57.80"

97°22’56.08" W

6.2

Bayview Resaca #2

26° 10’31 .67"

97°22’59.75" W

9.0

Willamar

26°23’16.56"

97°34’59.66" W

dry

Salt Marshes

Stover Point, LANWR

26° 13’01 .00"

97° 19’00.00" W

44.8

Spillway Crossing, LANWR

26° 16’00.00"

97°23’44.09" W

22.0

Large Marsh, LANWR

26° 12’50.79"

97° 19’52.06" W

20.5

Dry Marsh, LANWR

26° 13’00.39"

97° 19’02.46" W

dry

Osprey Point, LANWR

26° 13’58.32"

97°21’01.97" W

51.0

Laguna Atascosa Cayo, LANWR

26° 14’45.55"

97°25’13.12" W

22.0

Redhead Ridge, LANWR

26° 10’27.74"

97° 18’15.67" W

55.6

Rangerville #1, TPWD

26°05’ 17.22"

97°44’25.02" W

25.0

Rangerville *2, TPWD

26°05’08.78"

97°44’41 .65" W

22.0

Bayview Dry Marsh

26° 10’20.32"

97°22’55.51" W

33.0

Bayview Brine Marsh

26° 10’19.51"

97°23’59.73" W

67.5

Similarity of species composition among marshes was calculated using
Sorensen’s Coefficient of Community (Krebs 1999). Species importance
value was used as the measure of abundance for calculating species
diversity indices. Species diversity was assessed using the Shannon
diversity index (Brower et al. 1998; Krebs 1999). Evenness was deter¬
mined as the ratio of heterogeneity (H') to maximum heterogeneity (H'
max) (Brower et al.; Krebs 1999). One-way analysis of variance was
used to compare species richness, species diversity and evenness among
the three kinds of marshes (Sokal & Rohlf 1981). Nomenclature follows
Jones et al. (1997). Common names follow Hatch et al. (1999).

When surface water was present, salinity readings were obtained with
a temperature compensated hand-held refractometer (Table 1). Marshes
were classified as freshwater (0.0 to 0.5 ppt), brackish water (0.5 to
17.0 ppt) or saltwater (> 17.0 ppt).

JUDD & LONARD

107

Results

Freshwater marshes. — A total of 81 species were present in the six
marshes (Table 2). Species richness per marsh ranged from 15 to 31.
No species occurred in all of the marshes, but five species, Cy perns
articulatus (jointed flatsedge), Urochloa maxima (Guineagrass),
Paspalum lividum (longtom), Polygonum pensilvanicum (pink smart-
weed) and Typha domingensis (narrow-leaf cattail) were present in five
marshes. The introduced grass, U. maxima , was found only in the last
interval of transects where the marsh graded into an upland shrub-
grassland community. Tree seedlings and scattered shrubs including
Acacia famesiana (huisache), Celtis laevigata (sugar hackberry),
Ipomoea camea (shrubby morningglory) , Mimosa asperata (black
mimosa), Parkinsonia aculeata (retama), Salix exigua (sandbar willow)
and S. nigra (blackwillow) were present occasionally in the marshes.

There was a low degree of community similarity among the marshes
(Table 3). Coefficients of similarity ranged from 0.103 to 0.525.
Resaca de la Palma and Cattail Lake at Santa Ana National Wildlife
Refuge (SANWR) were the only marshes that had a coefficient of
similarity greater than 0.500. The mean of 15 coefficients of similarity
was 0.322 ( SD = 0.116). Clearly, there were marked differences in
species composition of freshwater marsh communities.

Each of the freshwater marshes had a different dominant species
(Table 4) and only a few species were responsible for most of the cover.
Indeed, the first six species in importance contributed from 72.6% to
96.4% of the relative cover. As with the flora in general, there was low
similarity among the marshes in the species making up the six most
important species. If each of the six most important species was
different in the six marshes, a total of 36 different species was possible;
however, 24 different species or 67% of the maximum diversity were
found. Nineteen of the 24 species occurred in two or more marshes and
12 occurred in three or more marshes.

Brackish water marshes. — Eighty-one species were present in nine
brackish marshes (Table 5). Species richness per marsh ranged from 7
to 24. No species occurred in all of the marshes, but Borrichia
frutescens occurred in eight marshes (all but Tio Cano #2). No other
species occurred in more than six of the marshes (Table 5). There was
a low degree of species similarity among most of the marshes (Table 6).
The exception was the two resacas at Palo Alto National Battlefield,
which had 66.7% of their species in common. These two sites were
separated by less than 0.5 km of coastal prairie. Thus, the similarity of

108

THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 2, 2004

Table 2. Species present in freshwater marshes in the Rio Grande Delta. 1 = Paso Real,
2 = Russelltown, 3 = Resaca de la Palma, 4 = Audubon Sabal Palm Sanctuary, 5 =
Cattail Lake and 6 = Willow Lake.

Species

2 3 4 5

Acacia farnesiana
Alternanthera paronychioides
Amaranthus sp.

Ambrosia psilostachya
Ammania coccinea
Bacopa monnieri
Bothriochloa laguroides
Cardiospermum halicacabum
Celtis laevigata
Chlorocantha spinosa
Chromolaena odorata
Clematis drummondii
Cocculus diversifolius
Commelina erecta
Croton sp.

Cucumis melo
Cynodon dactylon
Cyperaceae: unidentified
Cyperus articulatus
Cyperus digitatus
Cyperus elegans
Cyperus ochraceus
Cyperus odoratus
Cyperus rotundas
Cyperus virens
Cyperus sp. (1)

Cyperus sp. (2)

Dichanthium annulatum
Dichanthium aristatum
Dichanthium sp.

Eclipta prostrata
Echinochloa colona
Echinochloa muricata
Echinodorus beteroi
Eleocharis austrotexana
Eleocharis interstincta
Eleocharis parvula
Eleocharis sp.

Eragrostis reptans
Eriochloa punctata
Helianthus annuus
Heteranthera dubia
Ipomoea amnicola
Ipomoea carnea
Iva annua
Lemna sp.

Leptochloa fusca
Leptochloa nealleyi
Leptochloa panicea
Ludwigia octovalvis
Ludwig ia repens
Malachra capitata
Malvastrum coromandelianum
Marsilea vestita
Mikania scandens

X X

XXX

XX X XXX XX X XX XX X XX

JUDD & LONARD

109

Table 2. Continued.

Species

Mimosa asperata

Panicum hirsutum

Parkinsonia aculeata

Paspalum denticulatum

Phyla nodiflora

Physalis sp.

Pluchea purpurascens

Poaceae: unidentified

Polygonum densiflorum

Polygonum pensylvanicum

Prosopis reptans

Ricinus communis

Rubus riograndis

Salix exigua

Salix nigra

Schoenoplectus californicus

Sesbania herbacea

Sida sp.

Solanum americanum

Solanum campechiense

Sorghum halepense

Spermacoce glabra

Symphyotrichum divaricatum

Typha domingensis

Urochloa maxima

Vigna luteola

Table 3. Comparison of Sorensen’s community similarity coefficients among freshwater
marshes in the Rio Grande Delta. 1 = Paso Real, 2 = Russelltown, 3 = Resaca de la
Palma, 4 = Audubon Sabal Palm Sanctuary, 5 = Cattail Lake and 6 = Willow Lake.

1 2

Sites

4 5

Sites 4

0.370

0.300 0.370

0.178 0.103

0.311

0.361 0.218

0.525

0.217

0.491 0.298

0.415

0.263 0.407

their vegetation is not surprising. Coefficients of similarity for brackish
marshes ranged from 0.098 to 0.667 (Table 6). The mean of 36 coeffi¬
cients was 0.258 ( SD = 0. 123). Thus, the mean similarity for brackish
marshes was even less than for freshwater marshes.

Typha domingensis was the dominant species in three brackish
marshes (Table 7) and it was a co-dominant in a fourth. Bads tnaridma
was the dominant species in two brackish marshes. The six most
important species accounted for most of the cover (Table 7). Indeed,
the six most important species accounted for 88.0 to 99.8% of the

110

THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 2, 2004

Table 4. Comparison of species importance among freshwater marshes of the Rio Grande
Delta. Freq. = frequency, Rel. Freq. = relative frequency, Rel. Cov. = relative cover,
Imp. Val. = importance value (sum of relative frequency and relative cover).

Marsh

Species

Freq.

Rel.

Freq.

Cover

Rel.

Cov.

Imp.

Val.

Paso Real

Cyperus ochraceus

15.2

21.36

25.4

40.6

Eleocharis austrotexana

11.6

17.21

20.5

32.1

Polygonum densiflorum

10.7

14.83

17.7

28.4

Heteranthia dubia

8.0

11.23

13.4

21.4

Leptochloa fusca

10.7

7.05

8.4

19.1

Schoenoplectus californicus

24 additional species

2.7

Total

4.77

83.95

5.7

8.4

Russelltown

Urochloa maxima

9.9

21.99

24.0

33.9

Cyperus odoratus

8.5

20.87

22.8

31.3

Typha domingensis

11.3

12.62

13.8

25.3

Paspalum denticulatum

7.0

7.37

8.0

15.0

Mikania scandens

8.5

3.53

3.9

12.4

Eriochloa punctata

18 additional species

5.6

Total

3.59

91.37

3.9

9.5

Resaca de

Panicum hirsutum

84.8

17.9

36.11

37.5

55.4

la Palma

Typha domingensis

72.7

15.4

20.87

21.7

37.1

Cardiospermum halicacabum

45.5

9.6

5.20

5.4

15.0

Paspalum denticulatum

24.2

5.1

7.38

7.7

12.8

Sesbania herbacea

27.3

5.8

4.75

4.9

10.7

Solanum campechiense

24 additional species

24.2

5.1

Total

3.93

96.25

4.1

9.2

Sabal Palm

Malachra capitata

100.0

22.4

24.02

28.7

51.1

Sanctuary

Panicum hirsutum

72.7

16.3

21.82

26.1

42.4

Echinodorus beteroi

54.5

12.2

14.18

16.9

29.1

Eleocharis sp.

36.4

8.2

10.27

12.3

20.5

Heteranthera dubia

45.5

10.2

4.05

4.8

15.0

Lemna sp.

9 additional species

27.3

6.1

Total

6.36

83.73

7.6

13.7

Cattail Lake

Typha domingensis

66.7

8.8

16.48

18.0

26.8

Malachra capitata

66.7

8.8

12.90

14.1

22.9

Schoenoplectus californicus

46.7

6.1

13.58

14.9

21.0

Paspalum denticulatum

66.7

8.8

11.07

12.1

20.9

Phyla nodiflora

66.7

8.8

8.55

9.4

18.2

Cucumis melo

25 additional species

66.7

8.8

Total

3.75

91.31

4.1

12.9

Willow Lake

Paspalum denticulatum

75.0

16.0

55.26

62.5

78.5

Malachra capitata

56.3

12.0

8.59

9.7

21.7

Bacopa monnieri

37.5

8.0

7.91

8.4

16.4

Cyperus ochraceus

43.8

9.3

3.61

4.1

13.4

Eleocharis parvula

43.8

9.3

0.28

0.3

9.6

Schoenoplectus californicus

17 additional species

18.8

4.0

Total

4.91

88.48

5.5

9.5

JUDD & LONARD

Table 5. Species present in brackish marshes in the Rio Grande Delta. 1 = Palo Alto #1 ,
2 = Palo Alto #2, 3 = LANWR Resaca, 4 = Olmito Resaca, 5 — Tio Cano #1,6 =
Tio Cano #2, 7 = Bay view Resaca #1,8 = Bay view Resaca #2 and 9 = Willamar.

Species

2 3 4 5 6 7 8

Ambrosia psilostachya

Andropogon glomeratus

Atriplex pentandra

Bacopa monnieri

Batis maritima

Bolboschoenus maritimus

Borrichia frutescens X

Chamaesyce serpens

Chara sp. X

Chlorophyta filaments X

Chromolaena odorata

Cissus incisa

Citharexylum berlandieri

Conoclinium betonicifolium

Cynodon dactylon

Cyperus articulatus X

Cyperus ochraceus

Cyperus sp.

Dalea scandens
Dichanthium sp.

Distichlis spicata

Echinodorus beteroi X

Eclipta prostrata

Eleocharis austrotexana X

Eleocharis interstincta
Eleocharis sp.

Eriochloa punctata
Eustoma exaltatum
Forestiera angustifolia
Funastrum cynanchoides
Gossypianthus lanuginosus
Havardia pallens
Heliotropium curassavicum
Heteranthera dubia
Hydrocotyle bonariensis
Ipomoea amnicola
Ipomoea sagittata
Isocoma drummondii
Iva annua

Karwinskia humboldtiana
Lemna sp. X

Leptochloa fusca
Leucophyllum frutescens
Limonium carolinianum
Lycium carolinianum X

Machaeranthera phyllocephala
Malachra capitata
Marsilea vestita X

Maytenus phyllanthoides
Melothria pendula
Mikania scandens
Mimosa asperata

X X

X XX

X X

XXX

X X
X

X X

X X
X

X X

112

THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 2, 2004

Table 5. Continued.

Species

Mimosa strigillosa
Monanthochloe littoralis

Monocotyledon: unidentified
Opuntia engelmannii

Panicum hirsutum

Parkinsonia aculeata

Paspalum denticulatum

Phyla nodiflora

Pluchea purpurascens

Poaceae: unidentified

Prosopis glandulosa

Prosopis reptans

Rumex chrysocarpus

Salix nigra

Schoenoplectus californicus

Schoenoplectus pungens

Seshania drummondii

Seshania herbacea

Sesuvium maritimum

Sesuvium sessile

Sesuvium verrucosum

Solanum elaeagnifolium

Spartina spartinae

Sporobolus virginicus
Sporobolus wrightii

Suaeda linearis

Symphyotrichum divaricatum

Typha domingensis

Urochloa maxima

Table 6.

Comparison of Sorensen’s

community similarity coefficients

among

brackish

marshes

the Rio Grande Delta.

1 = Palo Alto #1,2 = Palo Alto #2, 3 =

LANWR

Resaca, 4 :

= Olmito Resaca, 5 = Tio Cano #1,6 =

Tio Cano #2, 7 =

Bayview Resaca

#1, 8 =

Bayview Resaca #2 and 9

= Willamar.

Sites

0.667

0.216

0.268

0.154

0.216

0.217

Sites

0.211

0.167

0.133

0.468

0.235

0.250

0.098

0.279

0.333

0.182

0.129

0.300

0.333

0.293

0.222

0.273

0.300

0.276

0.258

0.200

0.154

0.480

0.111

0.176

0.489

0.450

0.250

0.205

0.143

relative cover except in the Olmito marsh where the top six species
contributed only 66.7% of the relative cover.

If each of the six most important species was different in the nine
marshes, a total of 54 different species was possible. Thirty-one
different species or 57.4% of the maximum diversity were found.

JUDD & LONARD

113

Table 7. Comparison of species importance among brackish marshes of the Rio Grande
Delta. Freq. = frequency, Rel. Freq. = relative frequency, Rel. Cov. = relative cover,
Imp. Val. = importance value (sum of relative frequency and relative cover).

Marsh

Species

Freq.

Rel.

Freq.

Cover

Rel.

Cov.

Imp.

Val.

Palo Alto

Typha domingensis

94.4

18.8

41.14

50.4

69.2

Borrichia frutescens

100.0

19.8

18.66

22.8

42.6

Eleocharis austrotexana

77.8

15.3

9.37

11.0

26.3

P asp alum denticulatum

38.9

7.7

6.06

7.2

14.9

Lycium carolinianum

55.5

11.1

1.53

1.9

13.0

Marsilea vestita

8 additional species

44.5

8.6

Total

1.95

82.66

2.4

11.0

Palo Alto

Eleocharis austrotexana

93.3

22.2

44.89

59.7

81.9

Spartina spartinae

40.0

9.5

13.99

18.8

28.3

Borrichia frutescens

53.3

12.7

6.05

8.6

21.3

Marsilea vestita

53.3

12.7

5.11

7.2

19.9

Echinodorus beteroi

53.3

12.7

2.85

3.5

16.2

Heteranthera dubia

7 additional species

26.7

6.3

Total

0.49

74.49

0.8

7.1

LANWR

Batis maritima

71.4

17.0

24.00

26.5

43.5

Resaca

Monanthochloe littoralis

48.6

11.6

26.37

29.2

40.8

Borrichia frutescens

68.6

16.3

12.28

13.6

29.9

Spartina spartinae

25.7

6.1

14.98

16.6

22.7

Sporobolus virginicus

40.0

9.5

3.06

3.4

12.9

Schoenoplectus californicus

16 additional species

22.9

5.4

Total

3.21

90.39

3.6

9.0

Olmito

Leptochloa fusca

83.3

13.2

12.90

20.9

34.1

Sesuvium sessile

66.7

10.5

10.04

16.3

26.8

Pluchea purpurascens

61.1

9.6

5.06

8.2

17.8

Paspalum denticulatum

33.3

5.3

4.87

7.8

13.1

Parkinsonia aculeata

55.6

8.8

2.59

4.2

13.0

Sesuvium maritimum

18 additional species

22.2

3.5

Total

5.76

61.77

9.3

12.8

Tio Cano

Typha domingensis

97.4

22.8

32.44

32.9

55.7

Schoenoplectus pungens

39.5

9.3

21.31

21.6

30.9

Iva annua

36.8

8.6

13.53

13.7

22.3

Lycium carolinianum

71.1

16.7

2.76

2.8

19.5

Leptochloa fusca

36.8

8.6

7.85

8.0

16.6

Borrichia frutescens

17 additional species

26.3

6.2

Total

8.90

98.70

9.0

15.2

Tio Cano

Typha domingensis

91.4

17.4

41.94

35.1

52.5

Eleocharis interstincta

82.9

15.8

32.22

27.0

42.8

Distichlis spicata

77.1

14.7

24.08

20.1

34.8

Lycium carolinianum

82.9

15.8

3.53

3.0

18.8

Eleocharis sp.

28.6

5.4

6.68

5.6

11.0

Symphyotrichum divaricatum
13 additional species

34.3

6.5

Total

1.75

119.55

1.5

8.0

Bayview

Batis maritima

87.5

20.0

21.79

29.0

49.0

Resaca #1

Borrichia frutescens

68.8

15.7

19.35

25.8

41.5

Suaeda linearis

56.3

12.9

8.10

10.8

23.7

Eriochloa punctata

12.5

2.9

9.13

12.2

15.1

Distichlis spicata

31.3

7.1

5.70

7.7

14.8

Pluchea purpurascens

12 additional species

43.8

10.0

Total

2.48

74.96

3.3

13.3

114

THE TEXAS JOURNAL OF SCIENCE- VOL. 56, NO. 2, 2004

Table 7. Continued

Marsh

Species

Freq.

Rel.

Freq.

Cover

Rel.

Cov.

Imp.

Val.

Bayview

Borichia frutescens

83.3

25.0

37.43

33.3

58.3

Resaca #2

Typha domingensis

66.7

20.0

41.07

36.5

56.5

Distichlis spicata

67.3

20.0

17.05

15.2

35.2

Spartinci spartinae

33.3

10.0

6.28

5.6

15.6

Bolboschoenus maritimus

33.3

10.0

3.45

3.1

13.1

Urochloa maxima

1 additional species

16.7

5.0

Total

6.88

112.48

6.1

11.1

Willamar

Sesuvium maritimum

60.0

23.1

22.51

44.4

67.5

Sesbania herbacea

22.0

8.3

8.17

16.1

24.4

Heliotropium curassavicum

34.1

13.0

4.62

9.1

22.1

Bacopa monnieri

14.6

5.6

5.17

10.2

15.8

Borrichia frutescens

17.1

6.5

2.95

5.8

12.3

Pluchea purpurascens

15 additional species

19.5

7.4

Total

1.21

50.66

2.4

9.8

Salt water marshes.— Seventy-three species were present in 11 salt
marshes (Table 8). Species richness per marsh ranged from 7 to 26.
No species occurred in all the marshes, but B. frutescens was present in
10. Batis maritima and Prosopis reptans occurred in nine marshes and
Sporobolus virginicus was present in eight. Coefficients of similarity
ranged from 0.049 to 0.690 (Table 9). The mean of 55 coefficients was
0.372 ( SD = .147). One-way analysis of variance of coefficients of
similarity among freshwater, brackish and salt marshes showed signifi¬
cant variation among the kinds of marshes (i.e., among groups), F =
7.994, 2 & 103 df P < 0.001. Pairwise comparisons revealed only
one significant difference; the mean coefficient of similarity for salt
marshes was significantly greater than that for brackish marshes, t —
3.851, 89 df,P< 0.001.

The first six species in importance (Table 10) contributed from 82.2
to 99.4% of the relative cover. Borrichia frutescens and Paspalum
vaginatum each was a dominant species in three marshes and S.
spartinae and S. virginicus each was the dominant species in two
marshes (Table 10).

There was greater similarity in the important species of salt marshes
than in freshwater or brackish marshes. A list of the six most important
species included only 23 different species or 34.8% of the maximum
diversity of 66 different species. Freshwater and salt marshes had no
dominant species in common (Tables 4 and 10), but brackish and salt
marshes shared two dominant species, B. frutescens and Sesuvium
maritimum (Tables 7 and 10). Freshwater and brackish marshes shared
one dominant species, T. domingensis (Tables 4 and 7).

JUDD & LONARD

115

Table 8. Species present in salt marshes in the Rio Grande Delta. 1 = Stover Point, 2 =
Spillway Crossing, 3 = Large Marsh, 4 = Dry Marsh, 5 = Osprey Point, 6 = Laguna
Atascosa Cayo, 7 = Redhead Ridge, 8 = Rangerville #1,9 = Rangerville #2, 10 =
Bay view Dry Marsh, 11 = Bay view Brine Marsh.

Species 123456789 10 11

Abutilon sp.

Allowissadula lozanii
Ambrosia psilostachya
Atriplex pentandra
Bacopa monnieri
Batis maritima
Bolboschoenus maritimus
Borrichia frutescens
Bothriochloa laguroides
Char a sp.

Chromolaena odorata
Clappia suaedifolia
Cressa nudicaulis
Croton sp.

Cynanchum barbigerum
Cynodon dactylon
Cyperus articulatus
Desmanthus virgatus
Dichanthium annulatum
Dichanthium aristatum
Dichanthium sericeum
Distichlis spicata
Echinocereus sp.

Eriochloa punctata
Gaillardia pulchella
Hcliotropium angiospermum
Heliotropium curassavicum
Ibervillea lindheimeri
Isocoma drummondii
Jatropha dioica
Leptochloa uninerva
Limonium carolinianum
Lycium carolinianum
Machaeranthera phyllocephala
Malvastrum amcricanum
Malvastrum coromandelianum
Maytenus phyllanthoides
Monanthochloe littoralis
Opuntia engelmannii
Opuntia leptocaulis
Panicum hallii
Paspalum vaginatum
Passiflora foetida
Pennisetum ciliare
Phyla nodiflora
Portulaca pilosa
Pluchea purpurascens
Prosopis glandulosa
Prosopis reptans
Rhynchosia americana
Rhynchosia senna
Ruppia maritima
Salicornia virginica
Sesuvium maritimum
Sesuvium portulacastrum

X X
X
X

X X
X

X X
X X X X
X X

X X X X X X
X X X X X

X X

X X X X X X

X X

X X X X
X X

XXX
X X

116

THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 2, 2004

Table 8. Continued.

Species

10 11

Sesuvium sessile

Sesuvium verrucosum

Setaria leucopila

Setaria parviflora

Sida sp.

Solarium americanum

Solarium eleagnifolium

Solarium triquetrum

Spartina spartinae

Sporobolus pyramidatus

Sporobolus virginicus

Sporobolus wrightii

X X

Suaeda linearis

Trixis inula

Typha domingensis

Urochloa maxima

Xylothamia palmeri

Yucca treculeana

Table 9. Comparison of Sorensen’s community similarity coefficients among salt marshes
in the Rio Grande Delta. 1 = Stover Point, 2 = Spillway Crossing, 3 = Large Marsh,
4 = Dry Marsh, 5 = Osprey Point, 6 = Laguna Atascosa Cayo, 7 = Redhead Ridge,
8 = Rangerville #1,9 = Rangerville #2, 10 = Bayview Dry Marsh, 11 = Bayview
Brine Marsh.

Site

5 6

9 10

0.483

0.458

0.571

0.593

0.458

0.526

0.478

0.500

0.533

0.556

Site 6

0.429

0.520

0.300

0.435

0.421

0.440

0.500

0.529

0.450

0.500

0.476

0.049

0.286

0.160

0.065

0.087

0.364

0.074

0.231

0.304

0.278

0.286

0.353

0.409

0.211

0.414

0.298

0.439

0.387

0.324

0.690

0.410

0.364

0.333

0.400

0.205

0.364

0.261

0.207

0.381

0.387

0.320

0.125

0.222 0.636

Comparison of species richness , species diversity and evenness among
marshes.— \ alues for species richness, species diversity, and evenness
are provided for each freshwater, brackish and salt marsh in Table 11.
One-way ANOVAs for each of these parameters showed no significant
differences among the kinds of marshes (Table 12). Freshwater and
brackish marshes shared 35 species (coefficient of similarity = 0.216).
Brackish and salt marshes had 30 species in common (coefficient of
similarity = 0.195), while freshwater and salt marshes shared only 19
species (coefficient of similarity = 0. 123). Freshwater and salt marshes
had only two important species in common, U. maxima and T.
domingensis.

JUDD & LONARD

117

Table 10. Comparison of species importance among salt marshes of the Rio Grande Delta.
Freq. = frequency, Rel. Freq. = relative frequency, Rel. Cov. = relative cover, Imp.
Val. = importance value (sum of relative frequency and relative cover).

Marsh

Species

Freq.

Rel.

Freq.

Cover

Rel.

Cov.

Imp.

Val.

Stover

Spartina spartinae

31.1

6.8

23.28

36.7

43.5

Point

Borrichia frutescens

60.6

13.3

5.46

8.6

21.9

Monanthochloe littoralis

36.1

7.9

8.51

13.4

21.3

Sporobolus virginicus

27.9

6.1

9.26

14.6

20.7

Prosopis reptans

45.9

10.0

0.94

1.5

11.5

Bothriochloa laguroides

26 additional species

14.7

3.2

Total

4.70

63.38

7.4

10.6

Spillway

Paspalum vaginatum

65.8

18.7

25.42

29.8

48.5

Crossing

Borrichia frutescens

44.7

12.7

12.30

14.4

27.1

Sporobolus virginicus

28.9

8.2

14.46

17.0

25.2

Satis maritima

42.1

11.9

8.78

10.3

22.2

Distichlis spicata

34.2

9.7

8.79

10.3

20.0

Bolboschoenus maritimus

20 additional species

28.9

8.2

Total

3.50

85.28

4.1

12.3

Large

Sporobolus virginicus

55.7

13.9

36.15

36.1

50.0

Marsh

Batis maritima

85.2

21.3

19.98

20.0

41.3

Monanthochloe littoralis

78.7

19.7

20.46

20.4

40.1

Borrichia frutescens

75.4

18.9

18.66

18.6

37.5

Lycium carolinianum

50.8

12.7

0.52

0.5

13.2

Sesuvium portulacastrum

10 additional species

18.0

4.5

Total

0.51

100.06

0.5

5.0

Dry Salt

Spartina spartinae

84.4

19.3

76.52

76.3

95.6

Marsh

Borrichia frutescens

87.5

20.0

10.24

10.2

30.2

Prosopis reptans

84.4

19.3

1.47

1.5

20.8

Monanthochloe littoralis

31.3

7.1

4.22

4.2

11.3

Salicornia virginica

21.9

5.0

1.70

1.7

6.7

Cressa nudicaulis

16 additional species

18.8

4.3

Total

0.66

100.27

0.7

5.0

Osprey

Borrichia frutescens

90.0

20.0

33.64

41.1

61.1

Point

Sporobolus virginicus

70.0

15.6

21.46

26.2

41.8

Monanthochloe littoralis

50.0

11.1

6.88

8.4

19.5

Typha domingensis

50.0

11.1

5.70

7.0

18.1

Batis maritima

60.0

13.3

2.14

2.6

15.9

Char a sp.

8 additional species

30.0

6.7

Total

1.82

81.81

2.2

8.9

Laguna

Paspalum vaginatum

65.4

14.8

31.5

31.7

46.5

Atascosa

Borrichia frutescens

57.7

13.0

16.38

16.5

29.5

Cayo

Bolboschoenus maritimus

61.5

13.9

15.02

15.1

29.0

Distichlis spicata

57.7

13.0

13.47

13.6

26.6

Suaeda linearis

23.1

5.2

7.95

8.0

13.2

Sporobolus wrightii

18 additional species

15.4

3.5

Total

4.26

99.25

4.3

7.8

Redhead

Sporobolus virginicus

75.0

16.2

35.18

39.2

55.4

Ridge

Sporobolus wrightii

54.2

11.7

20.68

23.1

34.8

Borrichia frutescens

75.0

16.2

14.15

15.8

32.0

Char a sp.

29.2

6.3

7.87

8.8

15.1

Batis maritima

45.8

9.9

4.50

5.0

14.9

Prosopis reptans

12 additional species

45.8

9.9

Total

1.77

89.72

2.0

11.9

118

THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 2, 2004

Table 10. Continued.

Marsh

Species

Freq.

Rel.

Freq.

Cover

Rel.

Cov.

Imp.

Val.

Rangerville

Paspalum vaginatum

69.0

37.7

29.63

53.1

90.8

Sesuvium maritimum

51.7

28.3

16.14

28.9

57.2

Sesuvium verrucosum

17.2

9.4

4.63

8.3

17.7

Pluchea purpurascens

13.8

7.5

2.82

5.1

12.6

Typha domingensis

13.8

7.5

0.87

1.6

9.1

Urochloa maxima

3 additional species

6.9

3.8

Total

1.36

55.80

2.4

6.2

Rangerville

Sesuvium maritimum

66.7

18.5

20.05

31.9

50.4

Sesuvium verrucosum

50.0

13.9

8.75

13.9

27.8

Borrichia frutescens

23.3

6.5

10.78

17.2

23.7

Sporobolus virginicus

30.0

8.3

6.97

11.1

19.4

Suaeda linearis

30.0

8.3

4.03

6.4

14.7

Typha domingensis

14 additional species

23.3

6.5

Total

4.50

62.80

7.2

13.7

Bayview

Borrichia frutescens

87.5

24.1

32.51

32.2

56.3

Brine

Distichlis spicata

62.5

17.2

27.46

27.2

44.4

Marsh

Ruppia maritima

50.0

13.8

25.11

24.9

38.7

Batis maritima

87.5

24.1

6.40

6.3

30.4

Sporobolus wrightii

37.5

10.3

8.41

8.3

18.6

Prosopis reptans

1 additional species

25.0

6.9

Total

0.26

100.98

0.3

7.2

Bayview

Borrichia frutescens

76.9

18.9

20.8

21.2

40.1

Dry Marsh

Distichlis spicata

69.2

17.0

19.36

19.7

36.7

Batis maritima

53.8

13.2

15.53

15.8

29.0

Char a sp.

30.8

7.5

14.42

14.7

22.2

Sporobolus wrightii

38.5

9.4

9.85

10.0

19.4

Typha domingensis

9 additional species

23.1

5.7

Total

7.20

98.26

7.3

13.0

Discussion

Only Judd & Lonard (2002) have provided information on species
diversity and evenness of Rio Grande Delta marshes and this is for only
one salt marsh and one brackish marsh. The marshes they studied are
included in the data set of this investigation. Information on species
richness is meager. White & Schmedes (1986) identified species
“typical” of each of the three marsh types rather than providing a list of
all species occurring in each kind of marsh. Thus, they do not provide
a measure of species richness. However, if one compares their list of
“typical” species with our group of important species (the number of
different species in the list of the six most important species), the
numbers are similar. For example, White & Schmedes (1986) identified
18 species typical of salt marshes and this study found 23 important
species. They report 26 typical species in brackish marshes and this

JUDD & LONARD

119

Table 11. Comparison of species richness (N), species diversity (H'), and Evenness (J')
among freshwater, brackish and salt marshes of the Rio Grande Delta.

Marsh

Freshwater Marshes

Paso Real

1.477

0.755

Russelltown

1.380

0.857

Resaca de la Palma

1.477

0.753

Audubon Sabal Palm Sanctuary

1.176

0.788

Cattail Lake

1.491

0.839

Willow Lake

1.362

0.735

Brackish Marshes

Palo Alto #1

1.461

0.729

Palo Alto #2

1.114

0.749

LANWR Resaca

1.342

0.760

Olmito Resaca

1.380

0.870

Tio Cano #1

1.362

0.753

Tio Cano #2

1.279

0.735

Bay view Resaca #1

1.255

0.803

Bayview Resaca #2

0.845

0.880

Willamar

1.322

0.766

Salt Marshes

Stover Point

1.505

0.779

Spillway Crossing

1.415

0.741

Large Salt Marsh

1.204

0.674

Dry Salt Marsh

1.342

0.621

Osprey Point

1.146

0.801

Laguna Atascosa Cayo

1.380

0.774

Redhead Ridge

1.255

0.763

Rangerville #\

0.954

0.681

Rangerville #2

1.301

0.798

Bayview Brine Marsh

0.845

0.884

Bayview Dry Marsh

1.176

0.837

Table 12. Analysis of variance for species richness, species diversity,
freshwater, brackish and salt marshes of the Rio Grande Delta.

and evenness

among

Parameter & Source
of Variation

F (Probability)

Species Richness (N)

Among Marshes

236.425

118.213

2.749 (P > 0.05)

Within Marshes

988.960

43.000

Total

1,225.385

Species Diversity (H')

Among Marshes

0.110

0.055

1.719 (P > 0.1)

Within Marshes

0.727

0.032

Total

0.837

Evenness (J')

Among Marshes

0.004

0.002

0.500 (P > 0.5)

Within Marshes

0.096

0.004

Total

0.100

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THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 2, 2004

study found 31 important species. White & Schmedes identify 26
species typical of freshwater marshes and this study found 24 are
important.

Clover (1937) identified 44 species associated with freshwater habitats
in the Lower Rio Grande Valley of Texas, but she did not list species
associated with brackish or salt marshes. The number of species she
lists for freshwater habitats is far greater than the number of typical
species for freshwater marshes reported by White & Schmedes (1986),
but far less than the 81 species this study found in freshwater marshes.
Only 14 of the 44 freshwater species Clover (1937) identified were
found in this study. Conversely, this study found 13 of the 26 species
White & Schmedes (1986) listed as occurring in freshwater marshes in
freshwater marshes and three others in brackish marshes and this study
found 17 of the 26 species they listed for brackish marshes in brackish
marshes and four others in salt marshes. This study found 13 of the 18
species they listed for salt marshes in salt marshes. Perhaps this study
found a lower percentage of the freshwater species identified by Clover
(1937) because there has been a longer time for changes in the flora
since her study than there has been since White & Schmedes’ (1986)
study.

Species composition among marshes of a given type such as fresh¬
water marshes is highly variable even within a relatively small area such
as the Rio Grande Delta. Jacobson & Jacobson (1989) found a similar
relationship among 18 salt marshes of the Maine coast. Despite the
variability in species composition, in most cases one can separate
freshwater marshes from salt marshes by the important species present
(especially the dominant species) . Only two important/dominant species,
T. domingensis and U. maxima , were common to freshwater and salt
marshes. Typha domingensis clearly exhibits a broad range of salinity
tolerance for the species was found in freshwater, brackish and salt
marshes. White & Schmedes (1986) list T. domingensis as a species
characteristic of freshwater marshes and they also found it in brackish
marshes, but they do not list it as one of the species occurring in salt
marshes in the Rio Grande Delta area. White & Schmedes (1986) do
not list U. maxima as a species associated with any of the three kinds of
marshes. This is likely because the species was uncommon in the Rio
Grande Delta area when they did their field investigations, i.e., prior to
1986. Today, U. maxima is found on the margins of freshwater, brack¬
ish and salt marshes and it invades freshwater and brackish marshes
when they begin to dry.

White & Schmedes (1986) noted that brackish marshes are transitional

JUDD & LONARD

121

between freshwater and salt marshes and contain some species typical of
both marsh types. This current study found that this was certainly so.
Of the 32 important species occurring in brackish marshes, 12 also were
important in freshwater marshes and 13 were important in salt marshes.
Typha domingensis and U. maxima were important in all three kinds of
marshes.

Species richness that was observed in Rio Grande Delta marshes
appears to be similar to species diversity in marshes distant from the
area. For example, Jacobson & Jacobson (1989) reported that species
richness of 1 8 salt marshes along the Maine coast ranged from 11 to 25
( x = 17.22, SD — 4.37). This study found that species richness in 11
Rio Grande Delta salt marshes ranged from 7 to 32 (x = 18.45, SD =
7.38). There was no significant difference in the means ( t = 0.569, 27
df,P> 0.5). Testing the general izability of the marsh species richness,
species diversity and evenness values obtained in this study awaits the
reporting of additional information from other areas of the Texas coast.

Acknowledgments

Financial support was provided, in part, by Texas Higher Education
Coordinating Board Advanced Technology Grant No. 003599-009-1997,
which is gratefully acknowledged.

Literature Cited

Brower, J. E., J. H. Zar & C. N. Von Ende. 1998. Field and Laboratory Methods for
General Ecology. WCB/McGraw-Hill. Boston, Massachusetts. U.S.A., 273 pp.
Brown, L. F., Jr., J. L. Brewton, T. J. Evans, J. H. McGowen, W. A. White, C. G. Groat
& W. L. Fisher. 1980. Environmental Geologic Atlas of the Texas Coastal Zone -
Brownsville - Harlingen Area. The University of Texas at Austin, Bureau of Economic
Geology, 140 pp 4- 9 maps.

Canfield, R. H. 1941. Application of the line interception method in sampling range
vegetation. Journal of Forestry, 39:388-394.

Clover, E. U. 1937. Vegetational survey of the lower Rio Grande Valley, Texas.
Madrono, 4:41-72, 77-100.

Hatch, S. L., J. L. Schuster & D. L. Drawe. 1999. Grasses of the Texas Gulf Prairies and
Marshes. Texas A&M University Press, College Station, 355 pp.

Jacobson, H. A. & G. L. Jacobson, Jr. 1989. Variability of vegetation in tidal marshes of
Maine. Canadian Journal of Botany, 67:230-238.

Jahrsdoerfer, S. E. & D. M. Leslie, Jr. 1988. Tamaulipan brushland of the Lower Rio
Grande Valley of South Texas: description, human impacts, and management options.
U. S. Fish and Wildlife Service, Biological Report 88 (36), 63 pp.

Johnston, M. C. 1955. Vegetation of the eolian plain and associated features of southern
Texas. Unpubl. Ph.D. dissertation. The Univ. of Texas at Austin, Texas, 167 pp.
Jones, S. D., J. K. Wipff & P. M. Montgomery. 1997. Vascular plants of Texas: a
comprehensive checklist including synonymy, bibliography, and index. Univ. Texas
Press, Austin, 404 pp.

122

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Judd, F. W. & R. I. Lonard. 2002. Species richness and diversity of brackish and salt
marshes in the Rio Grande Delta. Journal of Coastal Research, 18:751-759.

Judd, F. W., R. I. Lonard, J. H. Everitt, D. E. Escobar & M. R. Davis. 1997a. Using

multispectral videography to distinguish the pattern of zonation and plant species

composition in brackish water marshes of the Rio Grande Delta. Proceedings Fourth
International Conference on Remote Sensing for Marine and Coastal Environments
(Orlando, Florida, 17-19 March, 1997), pp. 621-629.

Judd, F. W., R. I. Lonard, J. H. Everitt, D. E. Escobar & M. R. Davis. 1997b. Using

multispectral videography to compare the pattern of zonation between brackish water

marshes and saltwater marshes of the Rio Grande Delta. Proceedings 16th Biennial
Workshop of Videography and Color Photography in Resource Assessment (Weslaco,
Texas, April 29 - May 1, 1997), pp. 394-405.

Krebs, C. J. 1999. Ecological Methodology, Menlo Park, California. Addison Wesley
Longman, 620 pp.

Lonard, R. I. & F. W. Judd. 1999. Vascular plants of the Rio Grande Delta marshes.
Proceedings 1999 Symposium of the Native Plant Society of Texas (October 14-17, 1999,
Harlingen, Texas), pp. 22-29.

Sokal, R. R. & F. J. Rohlf. 1981. Biometry. The Principles and Practice of Statistics in
Biological Research. 2nd Ed. W. H. Freeman and Company. New York, New York, 859

pp.

White, W. A., T. R. Calnan, R. A. Morton, R. W. Kimble, T. G. Littleton, J. H.
McGowen, H. S. Nance & K. E. Schmedes. 1986. Submerged Lands of Texas,
Brownsville - Harlingen Area: Sediments, Geochemistry, Benthic Macroinvertebrates, and
Associated Wetlands. The University of Texas at Austin, Bureau of Economic Geology,
138 pp. -I- 6 maps.

White, W. A. & K. E. Schmedes. 1986. Wetlands. Pp. 67-93, in White, W. A., T. R.
Calnan, R. A. Morton, R. W. Kimble, T. G. Littleton, J. H. McGowen, H. S. Nance,
and K. E. Schmedes (eds.), Submerged Lands of Texas, Brownsville - Harlingen Area:
Sediments, Geochemistry, Benthic Macroinvertebrates, and Associated Wetlands. The
University of Texas at Austin, Bureau of Economic Geology, 138 pp. 4- 6 maps.

FWJ at: ljudd@panam.edu

TEXAS J. SCI. 56(2): 123-130

MAY, 2004

PHYSIOLOGICAL TOLERANCE RANGES OF LARVAL
CAEN1S LAT1PENNIS (EPHEMEROPTERA: CAENIDAE)

IN RESPONSE TO FLUCTUATIONS IN DISSOLVED OXYGEN
CONCENTRATION, pH AND TEMPERATURE

Robert T. Puckett* and Jerry L. Cook

Department of Biological Sciences, Sam Houston State University
Huntsville, Texas 77341
* Current address :

Department of Entomology , Texas A&M University
College Station, Texas 77843-2475

Abstract. — Laboratory experiments were conducted to investigate the physiological
tolerance ranges of the mayfly Caenis latipennis (Ephemeroptera: Caenidae) from Tanyard
Branch Creek in Walker County, Texas in response to stepwise fluctuations in dissolved
oxygen concentrations, temperature and pH. Survivorship decreased slightly at a dissolved
oxygen concentration of 7.0 mg/L, while trial groups suffered a dramatic decrease in
survivorship at a dissolved oxygen concentration of 4.5 mg/L. Mean CTMax (Critical
Thermal Maximum) for 10 individuals was 37.8°C with a range from 36.7°C to 38.5°C.
Mean critical lower pH for three trials of 10 individuals was 2.56 and mean critical upper
pH for three trials of 10 individuals was 12.5.

Assessments of benthic macroinvertebrate communities provide
general information regarding the water quality of the streams that
support them once baseline information regarding specific streams has
been gathered (Edmunds et al. 1976; Hilsenhoff 1977; Barbour et al.
1999; Rabeni et al. 1999; Lydy et al. 2000). However, the ultimate
goal of managing stream quality through the practice of bioassessment
is the ability to make stream management decisions based on reference
data (chemical, physical and biological). These data are typically
gathered from a specific region to bypass the expense and time of
developing baseline information from each regional stream (Barbour et
al. 1999). The cost effectiveness of stream bioassessment versus
physical /chemical monitoring is realized only after this baseline informa¬
tion is gathered (Barbour et al. 1999).

A critical requirement of a regionally specific bioassessment program
is an understanding of the physiological tolerance ranges of the species
comprising the resident benthic macroinvertebrate community. While
information exists regarding species specific tolerance ranges, this in¬
formation is typically anecdotal and not empirically derived (Hilsenhoff
1977; 1982). In addition, many species have large geographical ranges

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THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 2, 2004

raising the possibility that a continuum of intraspecific physiological
tolerance ranges occur. This stresses the necessity for determining
regionally specific species tolerance ranges.

Caenis latipennis occurs throughout North America north of Mexico,
including south central Canada to extreme southern Texas with a disjunct
population in southern Mexico (Provonsha 1990). In a previous study,
streams from two neighboring counties in southeast Texas (Walker and
San Jacinto counties) were monitored monthly for a period of one year
regarding their ephemeropteran community diversity responses to
fluctuating physical /chemical parameters. Regression analysis of mayfly
diversity against fluctuation of stream quality values indicated that of the
eight parameters sampled throughout the period, dissolved oxygen,
temperature and pH show the greatest correlation with fluctuating mayfly
diversity (Puckett 2003).

The goal of this study was to determine the range of dissolved
oxygen, temperature and pH that C. latipennis can tolerate with the hope
that this information can be used in stream bioassessment practices
specific to Walker County streams. The techniques used here may
provide a model for further investigations into species specific tolerance
ranges. Although this is not an investigation into the potential intra¬
specific geographical physiological tolerance gradient mentioned above,
the data presented here could serve for comparison to similar values
obtained for C. latipennis in other areas of its distribution.

Materials and Methods

Caenis latipennis larvae were collected from Tanyard Branch Creek,
taken to the laboratory at Sam Houston State University and allowed to
acclimate to laboratory conditions over a period of approximately one
week. Mayflies were collected using a standard 0.8 m by 0.8 m kick
screen and were transferred to the laboratory in 4 dram vials containing
stream water. Larvae were housed in mesh bottomed containers that
were submerged in water from the stream in which they were collected.
Of the thirty individuals housed in each container, twenty were selected
(10 per trial and 10 per control) for both dissolved oxygen and pH
experiments. Individuals were selected from the remaining laboratory
population for critical thermal maximum (CTMax) experiments.

Dissolved Oxygen Tolerance— A 2 liter beaker was capped with a 1 .5
cm styrofoam disk that was cut to precisely fit the beaker mouth. Holes

PUCKETT & COOK

125

were then cut in the disk to accommodate the container that housed the
mayflies, the connector hose from a N2 cylinder and dissolved oxygen
meter (YSI® Dissolved Oxygen Meter-Model 55/12FT).

The containers that housed the mayflies during the trials were made
by first removing the bottoms of two 100 mL plastic cups. A 7.6 cm
by 7.6 cm piece of fine mesh was then stretched around the bottom
opening of one cup and forced into the second cup. Once taut, this
mesh provided an artificial substrate and allowed for a homogenous
mixing of water inside and outside of the container. The conical shape
of the cups also allowed for a tight fit into the hole in the styrofoam disk
which diminished the amount of diffusion of atmospheric oxygen. A
plunger to seal off the original opening of this container was built by
attaching a 12 cm section of Pyrex® glass cylinder to the center of the
removed cup bottom. During trials this plunger was placed into the cup
so that it fit snugly beneath the water line, again with the goal of
reducing atmospheric oxygen diffusion into the trial beaker. The entire
apparatus was placed on a Corning® stirrer /hot-plate. During trials the
stir bar revolved at approximately 68 rpm. Stirring the water during
trials was essential for the operation of the dissolved oxygen meter.

De-ionized water was used in all trials. Mayflies were placed in DI
water three hours before the start of each trial. During the trials
dissolved oxygen was removed by purging the water slowly with
gaseous nitrogen to lower oxygen levels by 0.5 mg/L increments. Each
02 level was held for 45 min. until lethal 02 levels were met. The time
interval of 45 min. was determined after subjecting a pre-trial group of
ten individuals directly to a dissolved oxygen concentration of 0.5 mg/L.
After 40 min. all individuals were dead. Control groups were setup in
an identical fashion excluding only the N2 purge. Ten individuals each
in trial and control groups were monitored. All other water parameters
remained constant during trials.

Thermal Tolerance.— Determination of lethal maximum temperature
levels was carried out in a similar apparatus as that described for
dissolved oxygen trials. However, in the temperature trials an aquarium
heater and oxygen pump/bubbler were added to the apparatus and the
nitrogen component removed. Additionally, the plunger described in the
dissolved oxygen trials was removed. Critical thermal maximum
(CTMax) trials rely on the observation of a trial endpoint that is specific
to the organism being studied (Lutter schmidt & Hutchison 1997). For

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THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 2, 2004

Caenis latipennis , observation of lack of righting response followed by
the mayfly’s inability to cling to the artificial substrate was always
followed immediately by death. Inability to cling to the artificial
substrate was used as an endpoint in these trials.

Temperature was raised 1.5°C/min. until the endpoint was observed.
A total of ten individuals were subjected to these trials. Each trial was
performed on one individual per trial while controls were simultaneously
run and held at room temperature. As in dissolved oxygen trials,
de-ionized water was used. Trial and control individuals were allowed
the same acclimation period of approximately 3 hours. All other water
parameters remained constant during trials.

pH Tolerance.— pH trials were also carried out in closed beakers.
However, in these trials 1 liter beakers were used to minimize chemicals
necessary to accomplish stepwise manipulation of pH. Mayflies were
housed as described above.

Three trials were run in which a group of 10 individuals were
subjected to stepwise fluctuations of pH (both up and down) starting at
a pH value of 8.0. Separate trial groups were used for each trial. pH
levels were manipulated by titration with 2nHC1 (pH decrease) and
2NNaOH (pH increase). Levels were raised or lowered by half a pH
unit per hour. The time period of one hour was decided upon after
subjecting a pre-trial group of 10 individuals to water with a pH value
of 2. In just under an hour all individuals were dead. VWR Scientific
Products® benchtop pH meters (Model SB21) were used to monitor pH
levels during trials. Stream water was used in these trials rather than
de-ionized water as a result of discrepancy between the pH levels of
stream and de-ionized water. Death was signaled by individuals bending
at the first abdominal segment accompanied by an inability to remain
attached to the artificial substrate. Control groups of ten individuals
were run simultaneously. All other water parameters remained constant
during trials.

Results

Dissolved Oxygen Tolerance. — When exposed to stepwise reduction
of dissolved oxygen, survivorship of Caenis latipennis showed a subtle
decrease once a dissolved oxygen concentration of 7.0 mg/L was
reached. However, a dramatic decrease in survivorship was observed
after dissolved oxygen concentration levels were reduced to 4.5 mg/L
(Fig. la). Mortality continued to increase with relative dissolved

PUCKETT & COOK

127

D.O. Concentration (mg/I)

Figure 1 . Survivorship of three Caenis latipennis (a) dissolved oxygen tolerance threshold
trials, (b) pH decrease trials (One-way ANOVA on ranks [P=0.795]) and (c) pH increase
trials (One-way ANOVA on ranks [P= 1 .0001).

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THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 2, 2004

oxygen reduction with no individuals surviving below 1.5 mg/L.
Percent survivorship of the control groups during trials 1 , 2 and 3 were
80%, 90% and 100% respectively.

Thermal Tolerance.— CTMax trials show that the average upper
critical temperature for Caenis latipennis is 37.8 °C. All ten individuals
subjected to CTMax trials died between 36.7°C and 38.5 °C. The
critical thermal maximum temperature of individuals in these trials was
well above the maximum temperature value recorded in the stream
during the monitoring period (22.3°C). Controls were run simul¬
taneously at a temperature of 24.5 °C with no mortality.

pH Trials.— The critical lower pH level under which Caenis latipennis
could not survive was 2.5 (Fig. lb). In two of the three trials all
individuals were alive after being exposed to stepwise decrease of pH to
a level of 3.0 with 100% mortality after exposure to the same water at
a pH of 2.5. During the third trial 40% of the individuals died at pH
of 3.0 with the remaining individuals dying at a pH of 2.5. The lowest
pH value recorded from a stream during the monitoring period was 7.7.
Controls groups were run during the trials in a sample of the same water
that was used for trial groups. This water maintained a pH of 8.2 from
collection through the end of trials. No mortality was recorded in the
control groups.

The critical upper pH level above which Caenis latipennis could not
survive was 12.5 (Fig. lc). All individuals in each of three trials were
alive after being exposed to stepwise increase of pH to a level of 12.0,
after which at a pH value of 12.5 all three groups experienced 100%
mortality. The highest pH value recorded during the monitoring period
was 8.6. Control groups were run during the trials at a pH of 8.2 in
which no mortality was recorded.

Discussion

Caenis latipennis can cope with dramatic fluctuations in pH, dissolved
oxygen, and temperature. It is very unlikely that under natural
conditions C. latipennis larvae would be exposed to water quality
parameter values that would fall outside of the tolerance values
determined in the laboratory. This suggests a species that should be
considered extremely tolerant of a wide range of values pertaining to the
water quality parameters investigated in this study. This information is
in agreement with previously published pollution tolerance values
regarding C. latipennis by Hilsenhoff (1987).

PUCKETT & COOK

129

The unlikelihood that the values of the parameters investigated here
should, in natural systems, fall outside of this species range of tolerance
suggests that the utility of C. latipennis as an indicator of stream quality
is limited. However, when found in systems of low mayfly diversity
this species and others found to be similarly tolerant could serve as
valuable predictors of acute stream perturbation. At best, C. latipennis
should be assigned little weight when included in stream assessments
based on some biological index such as Hilsenhoffs Biotic Index.

The relative ease with which the range of tolerance values regarding
the parameters investigated were obtained suggests that empirically
derived tolerance ranges for most Ephemeropteran species can be
determined. Due to general similarities in morphology, life history, and
ecological requirements, it is likely that these laboratory methods could
also be used to gather data regarding physiological requirements of other
stream macroinvertebrates such as the orders Plecoptera and Trichop-
tera. With specific data regarding true tolerance ranges of these insects
and other stream invertebrates, bioassessment practices can be ap¬
proached and interpreted with greater accuracy and relied upon with
greater confidence.

Acknowledgments

We thank The Texas Academy of Science for partial funding of this
project through the 2002 student research award. For use of equipment
we thank Dr. Bill Lutter schmidt, Dr. Andrew Dewees and Dr. Jack
Turner. Special thanks to Brandon Lowery for help in specimen
collection.

Literature Cited

Barbour, M. T., J. Gerritsen, B. D. Snyder & J. B. Stribling. 1999. Rapid Bioassessment
Protocols for Use in Streams and Wadeable Rivers: Periphyton, Benthic

Macroinvertebrates and Fish, Second Edition. EPA 841-B-99-002. U.S. Environmental
Protection Agency; Office of Water; Washington D.C., 339 pp.

Edmunds, G. F., Jr., S. L. Jensen & L. Berner. 1976. The mayflies of North and Central
America. Univ. Minnesota Press, Minneapolis. 330 pp.

Hilsenhoff, W. H. 1977. Use of arthropods to evaluate water quality of streams. Technical
Bulletin Wisconsin Department of Natural Resources 100:1-15.

Hilsenhoff, W. H. 1982. Using a biotic index to evaluate water quality in streams.
Technical Bulletin Wisconsin Department of Natural Resources, 132:1-22.

Hilsenhoff, W. H. 1987. An improved biotic index of organic stream pollution. Great
Lakes Entomol . , 20:31-39.

Lutterschmidt, W. I. & V. H. Hutchison. 1997. The critical thermal maximum: history and
critique. Can. J. of Zool., 75:1561-1574.

130

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Lydy, M. J., C. G. Crawford & J. W. Frey. 2000. A comparison of selected diversity,
similarity, and biotic indices for detecting changes in benthic-invertebrate community
structure and stream quality. Arch, of Environ. Contam. Toxicol., 39:469-479.

Provonsha, A. V. 1990. A revision of the genus Caenis in North America (Ephemeroptera:
Caenidae). Trans. Am. Entomol. Soc., 116:801-884.

Puckett, R. T. 2003. Bioassessment potential and water quality tolerance thresholds of
larval ephemeroptera in southeast Texas streams. Unpublished M.S. thesis, Sam Houston
State Univ., Huntsville, Texas, 74 pp.

Rabeni, C. F., N. Wang & R. J. Sarver. 1999. Evaluating adequacy of the representative
stream reach used in invertebrate monitoring programs. J. N. Am. Benth. Soc.,
18:284-291.

RTP at rpuck@tamu.edu

TEXAS J. SCI. 56(2): 131-140

MAY, 2004

NATURAL HISTORY OF THE SOUTHERN PLAINS WOODRAT
NEOTOMA MICROPUS (RODENTIA: MURID AE)

FROM SOUTHERN TEXAS

John R. Suchecki*, Donald C. Ruthven, III, Charles F. Fulhorst
and Robert D. Bradley*

* Department of Biological Sciences
Texas Tech University, Lubbock, Texas 79409-3131 ,

Chaparral Wildlife Management Area, P.O. Box 115
Artesia Wells, Texas 78001 and
Department of Pathology
UT Medical Branch, Galveston, Texas 77555

Abstract. — One hundred forty-eight middens of the southern plains woodrat {Neotoma
micropus ) were excavated from eight study sites on the Chaparral Wildlife Management Area
in southern Texas. Several parameters were examined within and between study sites,
including sex and age of individuals, demographics of occupancy, and distance between
middens. One hundred seventy-seven individuals were captured, with significantly more
adult woodrats represented than any other age category. Ninety males and 87 females were
captured indicating an equal sex ratio. Analyses revealed that no difference existed in
distances between male middens or in distances between female middens. Together, the data
suggest no apparent patterns of social structure in woodrats at this study site.

The southern plains woodrat {Neotoma micropus) is distributed from
southeastern Colorado and southwestern Kansas through western Texas
into northern Mexico (Hall 1981; Wilson & Reeder 1993). In Texas,
N. micropus occupies the western two-thirds of the state, and generally
is associated with brushlands of the semi-arid region between the eastern
timberlands and the arid deserts to the west (Davis & Schmidly 1994).
Woodrats construct middens (nests) from sticks, cactus, and other debris
that are arranged into an above ground pile (Finley 1958; Birney 1973).
It is common to find aluminum cans, spent ammunition casings, trash,
and livestock dung on or within a midden, giving woodrats the nickname
"packrat." Below ground (if soil composition/texture permits excava¬
tion), a midden usually contains an elaborate tunnel system. In this tun¬
nel system, woodrats store food and nest material, and avoid predation.
In areas where non- friable soils do not permit the excavation of tunnels,
woodrats often rely on crevices in rocks, decaying timber and canopies
of trees for housing. Virtually all middens, whether in trees or below
ground, have the characteristic mound of sticks over the opening.

Several studies have been conducted on the systematics and phylo¬
genetic relationships of woodrats (see Edwards & Bradley 2002). How-

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ever, only a few studies have examined natural history parameters.
These indicate that woodrats are solitary and territorial animals (Braun
1989; Conditt & Ribble 1997; Johnson 1952; Raun 1966) with size of
territories or home ranges most likely depending on density of individu¬
als and availability of food. Among the most detailed study, to date, is
the study by Conditt & Ribble (1997) conducted on N. micropus at a
research site in south central Texas.

From March 2001 to January 2003, woodrat middens were excavated
and occupants captured as part of an ongoing study examining the
ecology of the White Water Arroyo arenavirus. Although woodrats
were collected under a destructive sampling design, natural history
parameters and other life history traits were recorded during the study.
The objective of this study was to compare and contrast these natural
history attributes (density, distance between middens, sex ratio, number
of young, number of animals per midden, and age class distribution) to
that available from other studies of N. micropus , especially to those of
Conditt & Ribble (1997) and Henke & Smith (2000) whose study sites
were located approximately 160 km northeast and 175 km southeast,
respectively, of the study site examined during this study.

Materials & Methods

Study sites for this project were located on the Chaparral Wildlife
Management Area (CWMA; 28° 20’ N, 99° 25’ W) that consists of
6,500 ha in the Rio Grande Plains of southern Texas (Ruthven &
Synatzske 2002). The CWMA is located approximately 160 km south
of San Antonio, between Catarina and Artesia Wells, Texas on Highway
133. The CWMA occurs within Dimmit and La Salle counties with the
county border approximately bisecting the property. Soils typically are
classified as Duval Fine Sandy Loam (DYB) and Dilley Fine Sandy
Loam (DFC) (Stevens & Arriaga 1985). Average annual precipitation
is 55 cm with most precipitation occurring between the months of April
and September (Stevens & Arriaga 1985). Vegetation (McLendon 1991 ;
Ruthven & Synatzske 2002) includes woody species such as mesquite
{Prosopis glandulosa ) and granjeno ( Celtis pallida ), herbaceous species
such as Lehmann lovegrass ( Eragrostis lehmanniana) , fringed singal-
grass ( Brachiaria cilliatissima ) , and hairy grama ( Bouteloua hirsuta) as
well as a wide array of cactus species ( Opuntia sp.). Dominant plant
species coupled with climatic factors results in classification as a
semi-arid acacia-grassland or mesquite-grassland.

SUCHECKI ET AL.

133

Figure 1. Map depicting the locations of the eight midden sites examined in this study.
Dashed line depicts the county line separating Dimmit and La Salle counties and the
heavy black line depicts the boundaries of the Chaparral Wildlife Management Area.

The soil composition and availability of food and cover on CWMA
provide habitats capable of supporting large populations of woodrats
(Finley 1958; Raun 1966). The northern half of CWMA is relatively
more open and contains a higher concentration of grassland habitat,
whereas the southern half contains a greater concentration of brush.
Rotational grazing with cattle occurs yearly during the period October
through April. Fire is used throughout the property to control brush and
provide livestock and native species with food resources and cover.

Woodrats were captured (by hand) during the excavation of middens
located at eight different sites (Fig. 1). Sites were defined as an area
possessing suitable habitat for maintaining a high density of woodrats (a
high density was required for aspects of the arenavirus study). Sites
were selected using a predetermined protocol to provide a relative means
of providing a uniform density (high) among sites. Sites for this study
(0.2 ha) were circular with a 25 m radius. Sites were not located closer
than 500 m from any other site. Once a suitable area was selected, a
center point was determined and middens visible along a 25 m transect
(in each cardinal direction) were counted. If the number of middens
observed along transects was equal to or greater than 10, the site was
deemed suitable for excavation. If the number of middens was less than
10, a new site was selected and the protocol repeated. Excavation was

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Table 1. Comparison of age and sex across the eight midden sites by collecting date.
Roman numbers refer to midden sites. Number of individuals for each age class and sex
are in parentheses (males, females).

Site

Date

Number

Age Class

Adult

Subadult

Juvenile

Pup

Mar 2001

31 (15, 16)

(4, 6)

(0, 0)

(4, 3)

14 (7, 7)

Jun 2001

25 (13, 12)

(6, 7)

(6, 5)

(1,0)

0 (0, 0)

III

Oct 2001

23 (10, 13)

(7, 6)

(1,4)

(2, 3)

0 (0, 0)

Jan 2002

19 (8, 11)

(6, 8)

(2, 1)

(0, 2)

0 (0, 0)

Mar 2002

21 (10, 11)

(6, 7)

(1,0)

(2, 3)

2(1, 1)

Jun 2002

20(10, 10)

(6, 7)

(2, 1)

(2, 2)

0 (0, 0)

VII

Oct 2002

19 (11,8)

(6, 6)

(4, 0)

(1, 2)

0 (0, 0)

VIII

Jan 2003

19 (13, 6)

(10, 6)

(2, 0)

(1,0)

0 (0, 0)

Total

177 (90, 87)

104 (51, 53)

29(18, 11)

28(13, 15)

16(8, 8)

conducted four times per year (January, March, June and October) over
a two-year period (Table 1). Each site was excavated only once during
the study; and all sites were excavated during a single trip to circumvent
seasonal biases.

Every midden within the boundaries of each site was excavated,
regardless of appearance. Because of the potential for an extensive
tunnel system within a midden, every tunnel was excavated to its termi¬
nation point to ensure that all individuals were captured from the midden
or to determine if the midden truly was uninhabited. Universal Trans¬
verse Mercator (UTM) coordinates were recorded with a hand-held GPS
unit for each midden excavated regardless if midden was inhabited or
vacant. These coordinates were later used to map each site to establish
a geographical perspective (Fig. 2).

If an individual woodrat escaped during the excavation of a midden,
an immediate effort was made to recapture it. Excavation activities were
conducted during daylight hours when rodent activity was lowest (wood-
rats are nocturnal). Each captured woodrat was assigned a TK number
(Museum of Texas Tech University identification number), weighed,
sexed, aged, reproductive status determined and locality (UTM) record¬
ed. Ages were catagorized as adult, subadult, juvenile, and pup based
on molting pattern (adult versus subadult), size/mass (subadult versus
juvenile), and attachment to mammae (juvenile versus pup). Animals
were either sacrificed (voucher specimens deposited in the Museum at
Texas Tech University) or transported to the University of Texas Medi¬
cal Branch at Galveston, Texas for inclusion in a prospective study on
the biology of arenaviruses in N. micropus.

SUCHECKI ET AL.

135

Midden Site III

Figure 2. Map of Midden Site III. Distance between grid lines is 5 meters. Spatial
relationships between middens were constructed using UTM coordinates collected in the
field (maps are oriented using north and east corrdinants). The labels include age class,
gender, and museum identification number (TK) of the woodrats collected from the
middens. Abbreviations include: AM = adult male, SAM = subadult male, AF = adult
female, SAF = subadult female, and J = juvenile.

The Chi-square test (x2) and Student’s f-test were performed, among
midden sites and within midden sites, to test for statistically significant
differences in age, sex, distance from other middens, etc. For examin¬
ing differences between the distribution of adult male and female wood-
rats, a gender- specific centroid was calculated for each midden site using
UTM coordinates collected in the field. The distance of each midden
from the corresponding centroid was measured in meters, and the mean
of the adult male woodrat-centroid distances was compared to the mean
of the adult female woodrat-centroid distances using a RankSum test.
Middens that were co-occupied by adults of different sexes were not
included in this study.

Results

One hundred forty-eight middens were excavated and 177 individuals
were captured (Table 1). Five escapees, that were not recaptured,

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Table 2. Mean distances between middens occupied by adult male or adult female woodrats,
by site. Ranges are in parentheses.

Site

Number
of middens

Male

Mean distance

Number
of middens

Female

Mean distance

19.5(16.8-24.1)

14.2 (9.8-20.5)

7.9 (1.4-15.5)

8.2 (5.0-15.6)

III

8.8 (7.2-11.0)

11.4 (2.0-23.2)

14.0(10.6-17.2)

12.9 (5.0-17.1)

14.7(12.5-11.1)

9.9 (2.8-16.4)

7.3 (5.0-7.2)

7.7 (3.0-28.2)

VII

5.8 (4. 2-7. 2)

9.3 (3.6-13.6)

VIII

7.9 (3.6-13.9)

14.8(11.0-19.7)

occurred during the study. Number of captures by site ranged from 19
to 31 and number of middens per site ranged from 11 to 23.

Age— Individuals were separated into four age classes (adult, sub¬
adult, juvenile and pup) resulting in 104 adults (58.8% of the total
population), 29 subadults (16.4%), 28 juveniles (15.8%), and 16 pups
(9.0%) being captured. Comparison of age classes (Table 1) revealed
a difference in the number of individuals within age classes across sites
(x2= 90.39, df = 21, P < 0.001), with adults typically being more
numerous than either subadults, juveniles or pups. However, in Site I,
adults and pups were more numerous than subadults or juveniles and in
Site II, adults and subadults were more numerous than juveniles or pups.

Sex. — Ninety males (50.8% of the population) and 87 females
(49.2%) were captured (Table 1). A /-test revealed no difference
between the number of males and females across the eight middens ( t =
0.32, df = 15, P > 0.05) or in a comparison of sex by age class ( t =
0.35, df=3,P> 0.05). No differences (x2 = 100.49, df = 45, P >
0.05) were found between sexes by age class over the eight midden
sites.

Distances between middens. — Calculation of distances between mid¬
dens (nearest-neighbor distance) were calculated from UTM coordinates
as shown in (Fig. 2). Estimates from all study sites (Table 2) resulted
in a mean of 6.58 m (range: 1.70 - 14.12 m). Mean distance between
male middens for the eight study sites was 10.75 m (range: 7.23 - 16.40
m), whereas mean distance between female middens was 11.05 m
(range: 5.16 - 19.49 m). No significant difference in distance was
detected between each midden among the eight sites (x2, P > 0.05 for
each of the eight sites), between sexes within sites (/-test, P > 0.05 for
each of the eight sites) , or in mean differences between sexes among the

SUCHECKI ET AL.

137

Table 3. Average distances between middens occupied by adult woodrats and gender-specific
centroids, by midden site. The number of males or females captured is in parentheses.

Midden site

Gender

III

VII

VIII

Overall

Male

Female

16.9 (4)
15.7 (5)

15.3 (6)
17.8 (7)

20.7 (7)
20.3 (6)

18.0 (6)
22.6 (8)

20.2 (6)
18.1 (7)

10.9 (6)
16.6 (7)

16.0 (7)
14.8 (5)

16.3 (10)
20.2 (6)

18.5 (52)
16.8 (51)

eight sites (/ = 0.22, df = 7, P > 0.05). Middens containing both
adult males and adult females were excluded from this analysis, as it
was impossible to determine whether the male or female was the
primary occupant of the midden.

The means of midden-centroid distances of male and female woodrats
were 18.5 m (range: 3.9 - 32.6 m) and 16.8 m (range: 5.6 - 31.9 m),
respectively. The results of a RankSum test (Table 3) indicated that
there was no statistically significant difference (Type I error = 0.10)
between the mean midden-centroid distance of male woodrats and the
mean midden- centroid distance of the female woodrats.

Middens /site. — Average number of middens per site was 18.37. No
differences were identified between number of middens per site ( t =
0.00, df = 7, P > 0.05), number of male middens versus female
middens among sites (x2 = 3.13, df — 7, P > 0.05), or number of
male middens versus female middens within sites ( t = 0.27, df = xx,
P > 0.05). Site VIII contained the greatest number of middens (23),
whereas Site I had the fewest (11). Site I had the largest number of
individuals (31) and Sites IV, VII and VIII had the fewest (19).

Occupancy per midden— One hundred six of the 148 excavated
middens (71.6%) were occupied. Calculations of multiple occupancy,
(how many individuals of each age class and sex occupy the same
midden), indicated that adult females and their young were found
together on 27 (18.2%) occasions. Using number of pups as a baseline,
the average litter size is two (27 females with 54 pups). Adult females
and adult males were found in the same midden 13 (8.7%) times. The
greatest number of individuals found in a single midden was six and five
middens contained five individuals.

Discussion

Several parameters were examined and only age class structure varied
statistically by site, season or between years. The adult age class ( n —
104) contained the highest number of individuals and the pup age class

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contained the least ( n = 16). Interestingly, pups were collected only in
March indicating a peak reproductive effort in late winter or early
spring; however, the presence of juveniles during other months suggests
that some reproduction occurs throughout the year. In addition, this
time frame corresponded to the population peak in February reported by
Conditt & RIbble (1997). However, reproductive efforts appeared to
taper off more rapidly in this study than reported in Conditt & Ribble
(1997), where the number of lactating or pregnant females peaked at
50% in October.

Because of the idea that the woodrats might have a polygynous or
promiscuous mating system (Conditt & Ribble 1997), it was assumed
that the number of females collected would be more numerous than
males. As indicated, there was no significant difference in the overall
number of males (90) compared to females (87) or in any age class.
The ratio of adult males to females was 1:0.97; whereas, the study by
Conditt & Ribble (1997) reported a ratio of 1:1.16.

The social structure within the midden itself was another aspect of the
study that did not hold true with assumptions pertaining to woodrat
habits. The most surprising finding was that adult males and adult
females being captured within the same midden. Conditt & Ribble
(1997) never observed more than one adult woodrat in a midden at the
same time. However, during this study, an adult male and an adult
female were observed in 13 middens. There are at least two possibilities
to explain this. The simplest would be that the male was there solely for
mating purposes. Although this may be true, all middens were exca¬
vated during daylight hours, and N. micropus is a nocturnal species.
Because of this, several questions arise as to the social habits of N.
micropus. How long does courtship take place, perhaps they stay "over¬
day. " Second because of high densities of woodrat middens on CWMA,
perhaps adult males and females cohabitate. Parameters of this study do
not provide significant conclusions to these questions.

Because of the direct capture of all individuals throughout all midden
sites, one aspect of their natural history that could not be measured is
home range. Studies by Henke & Smith (2000) and Conditt & Ribble
(1997) that examined home range within N. micropus found the home
range of males to be 1696 m2 and 1829.2 m2, respectively. Female
home range was found to be significantly less at 188 m2 and 258.2 m2,
respectively. Although one could not calculate home ranges due to the
destructive sampling design of this study, the data are not consistent with
a harem mating system. Instead, maps of each midden site revealed no

SUCHECKI ET AL.

139

visible patterns that would support social structure regarding midden
placement or midden selection by males or females. In addition, if a
polygynous or promiscuous mating system existed, average distances
between male middens and average distances between female middens
should differ. For example, there should be a “standard” distance
between male middens and to a lesser degree for female midden dis¬
tances. Statistical tests failed to support this hypothesis.

In addition, the number of woodrats per hectare in this study was
110.6 and the number of middens per hectare was 92.5. The number
of adult males was 31.9 and the number of adult females was 33. 1 per
hectare. These numbers are much greater than that found (2.0 woodrats
per hectare in October to 5.5 per hectare in February) by Conditt &
Ribble (1997). One possible explanation for the large increase is that
this study was biased for high densities of woodrat middens; these
numbers obviously would be lower if sites had been selected at random.
Due to the large numbers of woodrats per hectare and abundance of
resources, home ranges of woodrats on CWMA are most likely not that
large. When superimposed (not shown) on a map of the midden sites
(produced in this study) , the home ranges reported by Conditt & Ribble
(1997) and Henke & Smith (2000) for a single individual would extend
well beyond the boundaries of the entire midden site. This is somewhat
surprising given the similarities in habitats and geographic proximity of
the three studies.

This study answered several questions regarding the natural history
of N. micropus. Because of suitable habitat conditions, CWMA is ideal
for sustaining large populations of woodrats. The large amount of food
and cover resources available to woodrats on CWMA enable populations
to not only survive but do so in such close proximity with each other
that early predictions on habits and social structure simply do not apply.

Acknowledgments

We thank D. S. Carroll, B. R. Amman, J. D. Hanson, F. M.
Mendez-Harclerode, S. A. Reeder, M. L. Haynie, N. D. Durish, L. K.
Longhofer, L. R. McAiley, A. Vestal, B. D. Cabbiness and J. G. Brant
(Texas Tech University) and C. Milazzo, Jr., M. L. Milazzo, M.
Cajimat, S. Gardner, J. Comer (University of Texas Medical Branch)
for assistance in field work. Special thanks to J. D. Hanson for
assistance with data analysis. D. R. Synatzske and other members of
Texas Parks and Wildlife Department at the CWMA provided important
logistical help. R. J. Baker and the staff at the Natural Science

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THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 2, 2004

Research Laboratory, Museum Texas Tech University provided assis¬
tance with specimen deposition. This research was supported by the
National Institutes of Health (grant DHHS A 14 1435-01) entitled
"Ecology of emerging arenaviruses in the southwestern U.S.".

Literature Cited

Birney, E. C. 1973. Systematics of three species of woodrats (genus Neotoma) in central
North America. Misc. Publ., Mus. Nat. Hist., Univ. Kansas Publ., 58:1-173.

Braun, J. K. 1989. Neotoma micropus. Mammalian Species, 330:1-9.

Conditt, S. A. & D. O. Ribble. 1997. Social organization of Neotoma micropus , the
southern plains woodrat. Am. Mid. Nat, 137(2): 290-297.

Davis, W. B., & D. J. Schmidly. 1994. The mammals of Texas. Texas Parks And
Wildlife Press, Austin, 338 pp.

Edwards, C. W. & R. D. Bradley. 2002. Molecular systematics of the genus Neotoma.
Mol. Phylo. Evol., 25(3): 489-500.

Finley, R. B., Jr. 1958. The wood rats of Colorado: distribution and ecology. Mus. Nat.
Hist., Univ. Kansas Publ., 10:213-552.

Hall, E. R. 1981. The mammals of North America. 2nd ed. John Wiley & Sons, New
York, vi + 601-1181 + 90.

Henke, S. E. & S. A. Smith. 2000. Use of aluminum foil balls to determine home ranges
of woodrats. Southwest. Nat., 45(2):352-355.

71(4):510-519.

Johnson, C. W. 1952. The ecological life history of the packrat, Neotoma micropus, in the
brushlands of Southwest Texas. Unpubl. M.S. Thesis, Univ. Texas, Austin. 115 p.
McLendon, T. 1991 . Preliminary description of the vegetation of south Texas exclusive of
coastal saline zones. Texas J. Sci., 43(1): 13-32.

Raun, G. G. 1966. A population of woodrats {Neotoma micropus) in southern Texas.

Bulletin of Texas Memorial Museum, 11:1-62.

Ruthven, D. C., Ill & D. R. Synatzske. 2002. Response of herbaceous vegetation to
summer fire in the western south Texas Plains. Texas J. Sci., 54(2): 195-210.

Stevens, J. W. & D. Arriaga. 1985. Soil Survey of Dimmit and Zavala Counties, Texas.

United States Department of Agriculture, Washington D.C.

Wilson, D. E. & D. M. Reeder. 1993. Mammal species of the world. 2nd ed. Smithsonian
Institution Press, Washington D.C., 1206 pp.

RDB at: robert.bradley@ttu.edu

TEXAS J. SCI. 56(2): 141-148

MAY, 2004

ADULT FORAGING BEHAVIOR
IN MEARNS’ GRASSHOPPER MOUSE,

ONYCHOMYS AREN1COLA (RODENTIA: MURID AE)

IS INFLUENCED BY EARLY OLFACTORY EXPERIENCE

Fred Punzo

Department of Biology
University of Tampa
Tampa, Florida 33606

Abstract.— Studies were conducted to assess the effects of early exposure to food-borne
olfactory cues and subsequent searching behavior and odor preferences in adult males of the
grasshopper mouse, Onychomys arenicola. Twenty-day old mice were randomly assigned
to 1 of 3 treatment groups: a control group (CG) was fed on crickets (Acheta domesticus ) and
mealworms ( Tenebrio molitor). Another group (EG) received an enriched diet of crickets,
mealworms, roaches ( Periplaneta americana), and commercial dog and cat chow. The IG
group received an impoverished diet consisting only of crickets. These feeding regimes
continued for 80 days. Mice were then presented with odor choice tests in a Y-maze
olfactometer. Mice from each treatment group were tested for their choices between known
and novel prey odors (NPO), and between known odors and a novel pure chemical odor
(NCO). Control mice exhibited a preference of 70% for the known prey odor (cricket) and
only 30% for the NPO (wolf spider, Hogna carolinensis). In contrast, EG mice showed a
significantly higher preference (70%) toward the NPO. Only 20% of the IG animals chose
the NPO. In addition, EG mice made decisions on which odor to investigate significantly
faster than CG or IG animals. These results indicate that O. arenicola relies on olfactory
cues when making decisions concerning prey choice during foraging bouts. They also
suggest that knowledge of olfactory cues associated with prey is not innate in this species,
but is acquired during early sensitive periods of development (olfactory imprinting). This
is the first demonstration of olfactory imprinting in a murid rodent within the genus
Onychomys.

Previous studies have shown that early olfactory experience can affect
the subsequent foraging behaviors or prey choice of adult predators
including insects (Chapman et al. 1987), spiders (Punzo & Kukoyi
1997), rock crabs (Rebach 1996), turtles (Punzo & Alton 2002), lizards
(Punzo 2003a), polecats (Apfelbach 1973), ferrets and other mustelids
(Apfelbach 1992), murid rodents (Berdoy & Macdonald 1991), shrews
(Churchfield 1990; Punzo 2003b) and canids (Weldon 1990). Further¬
more, a study on the ferret Mustela putorius showed that olfactory
imprinting may be involved because certain odors encountered by young
animals during sensitive periods can serve as acquired sign stimuli for

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THE TEXAS JOURNAL OF SCIENCE— VOL. 56, NO. 2, 2004

subsequent prey identification and selection (Apfelbach 1992). How¬
ever, little information is available on the effects, if any, of early
olfactory experiences on subsequent foraging behavior in murid rodents
(Frank & Heske 1992).

Mearns’ grasshopper mouse, Onychomys arenicola (Rodentia:
Muridae) is an inhabitant of low desert areas in west Texas. They
prefer foothills, xeric flats and mesquite-covered mesas with sandy soils
(Whitaker 1996), and feed primarily on a variety of arthropods and
small vertebrates as well as seeds (Horner et al. 1965; Brown & Zeng
1989; Punzo 2000). The purpose of the present study was to assess the
influence of early olfactory experience on subsequent searching behavior
and odor preferences of adults of O. arenicola.

Materials and Methods

All animals used in these experiments were the second or third
generation offspring of adults originally collected from several localities
within a 4 km radius of Redford, Texas (Presidio County) in 1999 and
2000. This area lies within the northern region of the Chihuahuan
Desert. The experimental protocol used in this study was similar to that
employed by Apfelbach (1978). To summarize, 10 newly weaned mice
were randomly assigned to each of three groups, all of which were fed
a diet of crickets {Acheta domesticus ) and mealworms ( Tenebrio molitor)
until they were 20 days old. After this time, each group was fed on a
different diet regime until the age of 80 days. A control group (CG)
continued to receive crickets and mealworms; another group (EG) was
fed an "enriched" diet consisting of crickets, mealworms, roaches
(Periplaneta americana) and commercial cat and dog chow (Ralston
Purina, St. Louis, MO). An impoverished group (IG) received only
crickets. In addition, to enhance olfactory deprivation, the IG group
was exposed to an artificial olfactory environment saturated with the
odor of geraniol. It has been reported that the continuous exposure to
a single predominant odor can mask the ability of an animal to experi¬
ence other environmental odors resulting in what has been termed a state
of olfactory deprivation (Weldon 1990).

Behavioral studies were conducted on adult males from the three

PUNZO

143

Figure 1. Diagram of the Y-maze olfactometer used in odor choice experiments. GT =
glass tubing; F = flowmeters; V = valves. Arrows indicate direction of air flow. See
text for details.

groups (n — 10/group) when they reached 7 months of age. These
animals were tested in a Y-maze olfactometer to determine if there was
any preference shown toward certain odor cues. Two tests were given
to each animal: one in which the subject was given a choice between a
known prey odor and a novel prey odor, and another test where the
choice was between a known prey odor and a novel pure chemical odor.
There was a 10 min delay between tests. The general procedure was
similar to that employed by Apfelbach (1992). To summarize, the
olfactometer consisted of a Y-maze constructed of plexiglass (Fig. 1)
connected to sources of odor via glass tubing (GT). The air and odor
flow were controlled through the use of flowmeters (F) located before
and after the odor saturators (odors). Teflon valves (V), located at each
end of the Y-maze, were used to control the direction of flow of the
odors. Test odors were randomly introduced into the left or right end
of the maze before a mouse was allowed to leave the start box. Test
odors consisted of a known prey odor (cricket) , a novel prey odor (wolf
spider, Hogna carolinensis) and a novel pure chemical odor (oil of
wintergreen) . At the start of each trial an individual mouse, food-
deprived for 72 hr, was placed into the start box and allowed to remain

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THE TEXAS JOURNAL OF SCIENCE— VOL. 56, NO. 2, 2004

90 n
80:

N P O NCO

Figure 2. Percent choice (percent of trials in which animals explored the novel odors) of
adult males of Onychomys arenicola toward novel prey (NPO) and novel chemical (NCO)
odors. Data show that EG animals (experienced an enriched diet) exhibited a greater
tendency to explore novel odors as compared to the control (CG) and impoverished (IG)
groups. Black bars = CG (control) group; stippled bars = enriched group (EG);
unshaded bars = impoverished group (IG).

there for a period of 10 min. The start box door was then lifted, and the
mouse was allowed to enter the maze. A record was made of which
arm of the maze was chosen (% choice) for each trial, as well as the
time (sec) needed for a mouse to make its decision. An arm was
considered chosen if the animal moved into it at least as far as point C
or F. All observations were made behind a one-way mirror to minimize
disturbance to the animals.

Data on odor preference tests and time needed to make a decision
were analyzed using Chi-Squared and Kruskal-Wallis tests (Sokal &
Rohlf 1995).

Results

The results of the odor preference tests are shown in Fig. 2. In the
choice condition of known prey odor (crickets) versus novel prey odor
(NPO; wolf spiders), control animals (CG) exhibited a preference of
30% toward the NPO, and 70% to the cricket odor. In contrast,

PUNZO

145

30n

NPO NCO

Figure 3. Amount of time (sec) required for males of Onychomys arenicola to make a
decision as to which odor to choose. Data are expressed as means + SD (n = 10/group).
Black bars = CG (control group); stippled bars = enriched diet group (EG); unshaded
bars = impoverished group (IG); NPO = novel prey odor; NCO = novel pure chemical
odor.

animals exposed to an enriched diet (EG) showed a preference of 70%
toward the NPO, whereas only 20% of the IG animals chose the NPO.
The differences between the CG and EG, and between CG and IG were
significant (P < 0.01). In addition, novel chemical odors (NCO) were
less attractive to these mice than were novel prey odors.

The time needed by these animals to make a decision as to which
odor to investigate is shown in Fig. 3. In the choice condition of known
prey odor vs. NPO, mice exposed to the enriched diet (EG) made
decisions significantly faster than controls (P < 0.01) and IG (P <
0.001) animals. Similar results were obtained when a novel chemical
odor (NCO) was presented rather than a NPO.

Discussion

These results indicate that the cricetid rodent Onychomys arenicola
utilizes olfactory cues when making decisions during foraging bouts.
They also suggest that knowledge of olfactory cues associated with prey
is not innate in this species, but is acquired during early periods of
development. This type of olfactory imprinting on cues associated with
prey or other food items has been reported for animals from a diversity

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of taxa including insects (Thorpe 1939; Chapman et al. 1987), spiders
(Punzo & Kukoyi 1997), turtles (Burghardt & Hess 1966; Punzo &
Alton 2002), lizards (Punzo 2003a), polecats (Apfelbach 1973), ferrets
(Apfelbach 1992), and murid rodents (Berdoy & Macdonald 1991). To
the author’s knowledge, this is the first demonstration of olfactory
imprinting in a murid rodent within the genus Onychomys.

It has been argued that the ability to imprint on specific environmental
cues during an early sensitive maturational period would allow an animal
to combine the advantages of hardwired specialist feeders with those of
generalists who rely to a greater extent on learning (Johnston 1982;
Stephens 1991). The situation whereby a predator is exposed to only a
small number of prey items during some early sensitive period of life
might facilitate the formation of an olfactory search image, thereby
focusing food searching behavior for specific prey (Burghardt 1993).
Thus, even though an animal may have the capacity to feed on a variety
of food types (broad trophic niche), by concentrating on a single,
abundant and reliable food encountered early in life, individuals would
minimize energy costs associated with trial-and-error learning while
benefiting from the increased foraging efficiency associated with having
a single search image to facilitate hunting. In these experiments,
grasshopper mice that were exposed to only a small number of prey
objects early in life, did not respond strongly to novel prey odors and
even less to a novel chemical odor, both of which convey less important
olfactory information.

Onychomys arenicola is found in xeric habitats, where seasonal
fluctuations in prey availability are common (Punzo 2000). Although it
is a generalist predator that feeds on a variety of arthropods, small
vertebrates and seeds (Horner et al. 1965; Brown & Zeng 1989;
Whitaker 1996), the ability to form an early search image associated
with one or a few prey types that may be more locally abundant and
available, would contribute to its overall fitness.

Acknowledgments

I thank R. J. Edwards, S. Jenkins, C. Lowell, G. Price and
anonymous reviewers for comments on an earlier draft of the
manuscript, L. Hane for assistance in procuring some of the research
literature, and A. Nardelli for assistance in maintaining the animals in

PUNZO

147

captivity. This study was supported by a Faculty Development Grant
from the University of Tampa.

Literature Cited

Apfelbach, R. 1973. Olfactory sign stimulus for prey choice in polecats (Putorius putorius) .
Zeitschrift Tierpsychologie, 33:273-281.

Apfelbach, R. 1978. A sensitive phase for the development of olfactory preference in
ferrets ( Mustela putorius). Zeitschrift Saugertierkiinde, 43:289-294.

Apfelbach, R. 1992. Ontogenetic olfactory experience and adult searching behavior in the
carnivorous ferret. Pp. 155-165, in Chemical signals in vertebrates. Vol. 6 (R. L. Doty
& D. Muller-Schwarze, eds.), Plenum Press, New York, 598 pp.

Berdoy, M. & D. W. Macdonald. 1991. Factors affecting feeding in rats. Acta Zoologica,
12:261-279.

Brown, J. H. & Z. Zeng. 1989. Comparative population ecology of eleven species of
rodents in the Chihuahuan Desert. Ecology, 70:1507-1525.

Burghardt, G. M. 1993. The comparative imperative: genetics and ontogeny of
chemorecpetive responses in natricine snakes. Brain, Behavior and Evolution, 41:138-
146.

Burghardt, G. M. & E. H. Hess. 1966. Food imprinting in the snapping turtle. Science,
151:108-109.

Chapman, R. F., E. Bemays & J. G. Stoffaland. 1987. Perspectives in chemoreception and
behavior. Springer, New York, 466 pp.

Churchfield, S. 1990. The natural history of shrews. Cornell University Press, Ithaca,
New York, 178 pp.

Frank, D. H. & E. J. Heske. 1992. Seasonal changes in space use patterns in the southern
grasshopper mouse, Onychomys torridus. Journal of Mammalogy, 73:292-298.

Horner, B. E., J. M. Taylor & H. Padykula. 1965. Food habits and gastromorphology of
the grasshopper mouse. Journal of Mammalogy, 45:513-535.

Johnston, T. D. 1982. The selective costs and benefits of learning: an evolutionary
analysis. Advances in the Study of Behavior, 12:65-106.

Punzo, F. 2000. Desert arthropods: life history variations. Springer, New York, 311 pp.

Punzo, F. 2003a. The effects of early experience on subsequent feeding responses in the
tegu, Tupinambis teguixin (Squamata: Teiidae). Journal of Environmental Biology,
24:23-27.

Punzo, F. 2003b. The response of the least shrew ( Cryptotis parva) to olfactory cues
associated with prey. Prairie Naturalist, 35:213-221.

Punzo, F. & L. Alton. 2002. Evidence for the use of chemosensory cues by the alligator
snapping turtle Macroclemys temminckii to detect the presence of musk and mud turtles.
Florida Scientist, 65:134-139.

Punzo, F. & O. Kukoyi. 1997. The effects of prey chemical cues on patch residence time
in the wolf spider Trochosa parthenus (Cahmberlin) (Lycosidae) and the lynx spider
Oxyopes salticus Hentz (Oxyopidae). Bulletin british Arachnological Society, 10:323-
326.

Rebach, S. 1996. Role of prey odor in food recognition by rock crabs, Cancer irroratus
Say. Journal of Chemical Ecology, 22:2197-2207.

Sokal, R. R. & F. J. Rohlf. 1995. Biometry. 3rd ed. W. H. Freeman, New York, 887 pp.

Stephens, D. W. 1991. Change, regularity, and value in the evolution of animal learning.

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Behavioral Ecology, 2:77-89.

Thorpe, W. H. 1939. Further studies on pre-imaginal olfactory conditioning in insects.

Proceedings Royal Society of London B, 127:424-433.

Weldon, P. J. 1990. Responses by vertebrates to chemicals from predators. Pp. 500-521
in Chemical signals in vertebrates. Vol. 5 (D. Macdonald, D. Muller-Schwarze & S. E.
Natynczuk, eds.), Oxford University Press, New York, 672 pp.

Whitaker, J. O., Jr. 1996. Field guide to North American mammals. Alfred Knopf, New
York, 936 pp.

FP at: tpunzo@ut.edu

TEXAS J. SCI. 56(2): 149-156

MAY, 2004

ROBOTICS REPEAT ABILITY AND ACCURACY:
ANOTHER APPROACH

Jan Brink, Bill Hinds* and Alan Haney

Department of Manufacturing Engineering Technology and
* Department of Mathematics , Midwestern State University
Wichita Falls, Texas 76308

Abstract.— Repeatability is one characteristic of a robot, which is of tremendous
importance. In this paper the concept of repeatability is clearly defined in terms of the
standard deviation of the random component of the error of a robot in returning to a taught
position and accuracy is defined in terms of the mean error as a function of three important
variables. Data used to estimate repeatability and accuracy were obtained from a full-
factorial experiment in which speed, payload and amount of axis movement were used as
independent variables. The robot used to furnish data for this research was a PUMA 560.
A regression model was developed to estimate the accuracy at various factor levels and the
repeatability was determined to be 0.0036 inches. The statistical analysis clearly indicated
that all three factors, as well as their interactions, affect the accuracy of the robot. The
regression model indicated that approximately 35% of the radial error variability was
explained by the linear model and 65% of the radial error was due to repeatability.

The performance of a robot is highly dependent upon both the
repeatability and the accuracy of the robot. Repeatability is the robot’s
ability to return to a previously taught point (Rehg 1985). Repeatability
is especially important in assembly applications of robots and has a
critical effect on product quality since product tolerances are decreasing
(Khouja & Kumar 1999). Specifications on robots are often obtained
from robot vendors, but the problem with the use of these data is that
the user does not know the conditions under which they are tenable. It
is therefore necessary to investigate the interaction among various robot
process variables and determine the conditions under which a given mix
of values can be achieved (Offodile & Ugwu 1991).

Repeatability and accuracy are often confused and rarely defined in
a clear and unambiguous way. Necessarily, both accuracy and repeata¬
bility must be estimated by using the error made by the robot when
trying to return to a previously taught point. This error is defined to be
the radial distance from the previously taught point to the point at which
the end effector comes to rest. The method for estimating accuracy and
repeatability in this research will depend upon errors obtained experi¬
mentally by varying the speed, the weight of the payload and the amount
of axis movement. More specifically, for any combination of the three
variables the accuracy will be defined as the mean of the distribution of

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errors for that combination. As a result of this definition, accuracy is
constant for any fixed combination of speed, weight and amount of axis
movement. Therefore, accuracy has no connection to the variability of
the distribution of errors. The repeatability of a robot does depend on
the variability of the distribution of errors. In fact, repeatability will be
defined to be equal to three times the standard deviation of the distribu¬
tion of errors.

The definitions of accuracy and repeatability in the above paragraph
indicate that the mean of the distribution of errors depends on the values
of the variables while the standard deviation does not. Therefore, the
variation in the errors due to changes in the mean as a result of changes
in the three input variables must be removed in order to estimate
accuracy and repeatability. The standard mechanism for this task is a
model for the means developed by using statistical techniques on data
obtained from a designed experiment.

Materials and Methods

The parameters speed, payload and percentage of axis movements
were varied on a PUMA 560 robot using different combinations to
estimate accuracy and repeatability. A conventional X-Y-Z Cartesian
coordinate measurement system was used. The points of movements to
the X, Y and Z gauges were found by driving each of the six axes to
different percentages of axis movements. Errors were measured using
precision gauges for the X, Y and Z coordinates. A test stand was
constructed for this experiment similar to the one discussed by Warnecke
& Schraft (1982). The test stand was securely clamped down to a table
that was leveled. The test stand allowed measurement of X, Y and Z
deviations using three Mitutoyo dial indicator gauges. The three gauges
used have flat faced contact plates. The resolution of the Mitutoyo
gauges used is 0.0001 inches with a 0.25 inch stroke. The deviations
were expected to be in the 0.001-0.004 inches range. The rule of “10”
was therefore applied. This means the gages have a resolution 10 times
the expected reading. The temperature in the laboratory was kept at a
constant 71° F which is very close to the desired 68° F for precision
measurements (DeGarmo et al. 1997).

The three parameters weight, speed and percent of movement in each
axis were varied at three different levels designated low, medium and
high. A total of 27 different combinations were used. The PUMA robot
used had six different axes.

BRINKS, HINDS & HANEY

151

Weight.— The payload of the PUMA robot used was 2.5 kg (5.5 lbs).
This did not include the gripper. Four “one” lb weights and two “0.5”
lb weights were used. A special designed fixture that can be attached
to the wrist was used for varying the weight. It included a precision
ground 0.5000 inch diameter + /- 0.0001 inch precision tooling ball.
The tooling ball probe has a small “negligible” weight. The probe was
locked in position so no movement was available in the X, Y and Z
direction. The following loads were used in this experiment: low (1.5
lbs * 30% of the payload), medium (3.0 lbs ~ 60% of the payload)
and high (4.5 lbs « 90% of the payload).

Speed. — Maximum speed of this robot was 0.5m/sec, which is equiva¬
lent to an external program speed of 100. The following speeds were
used: low (30% of the maximum speed), medium (60% of the maximum
speed) and high (90% of the maximum speed).

Percent of range in each axis.— The maximum range of motion for
each of the axes was as follows: Joint 1: 320 degrees (waist), Joint 2:
250 degrees (shoulder), Joint 3: 270 degrees (elbow), Joint 4: 280
degrees (wrist 1), Joint 5: 200 degrees (wrist 2) and Joint 6: 520 degrees
(wrist 3). The following ranges of motion were used: low (10% of the
total range), medium (30% of the total range) and high (50% of the total
range) . The three ranges of the total motion used in this study are given
in Table 1. The 50% axis movement was not exceeded because the
return approach of the robot would have been unpredictable.

The robot was operated for a 15 minute warm up period before the
data gathering began. The point called GAUGE to which the end
effector was programmed to return was located near one of the extreme
points of the axis system. This extreme point was determined by
rotating joints 1, 3 and 5 of the robot the maximum amount in the
negative direction and joints 2, 4 and 6 the maximum in the positive
direction. The fixture with the three gauges was located at the point
called GAUGE and contact was made with the tooling ball to accurately
zero the three gauges. The PUMA 560 Victor Assembly Language was
used to create a program that drove the end effector to one of the three
locations determined by the chosen values for the variable, amount of
axis movement, and returned it to the point GAUGE. This movement
was repeated ten times for each of the twenty-seven combinations for
levels of speed, weight and amount of axis movement. The radial error

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Table 1 . Ranges of motion used for each of the six axes for each of the three levels of axis
movement.

Low (10%)

Medium (30%)

High (50%)

Joint 1 : 32 degrees

Joint 1 : 96 degrees

Joint 1 : 160 degrees

Joint 2: 25 degrees

Joint 2: 75 degrees

Joint 2: 125 degrees

Joint 3: 27 degrees

Joint 3: 81 degrees

Joint 3: 135 degrees

Joint 4: 28 degrees

Joint 4: 84 degrees

Joint 4: 140 degrees

Joint 5: 20 degrees

Joint 5: 60 degrees

Joint 5: 100 degrees

Joint 6: 52 degrees

Joint 6: 156 degrees

Joint 6: 260 degrees

was measured each time the tooling ball returned to the point GAUGE.
The total of 270 data measurements met the minimum for the twenty-
seven factor level combinations according to the ANSI/RIA R 15. 02-2
standard (ANSI 1992).

Results and Discussion

There were 10 measurements taken at each of the 27 factor level
combinations. Therefore, the experiment is considered a full -factorial
experiment with 10 replications. The response variable was the radial
distance R from the point gauge to the location of the center of the
tooling ball. This distance was computed from the errors in the X, Y
and Z directions by R = (X2 + Y2 + Z2),/2. After the experiment was
designed and the 270 data points were obtained, data analysis was
performed to determine if the three variables used in the experiment
were all significant in determining the mean of error R. The analysis
of the data using the Minitab software package yielded the main effects
plots shown in Figure 1 . These main effects plots indicate that each of
the three variables was significant in determining the mean error. In
general, the mean error was increased when any of the variables were
changed from their medium or zero setting which indicated a quadratic
relationship. Further evidence of the influence of the variables can be
seen in Figure 2 which shows a graph of the error data in groups of ten
replicates. This graph clearly indicates that the replicates produced
tightly grouped errors but changes in levels of the three factors produced
large changes in the magnitudes of the errors. Much of the variability
in the values of the errors reflects changes in the factor levels. In order

BRINKS, HINDS & HANEY

153

Figure 1 . Main Effects Plot for R. The mean radial error is given as a function of each of
the three factors at three levels as used in the study.

Order of Observation

Figure 2. Radial Errors in Replicate Groups. The factor levels were changed after each
group of ten observations. The data represent 270 observations with 27 different factor
level combinations.

to get to the component of the data that reflects the repeatability of the
robot, regression techniques with a linear model were used to remove
the variation due to changes in factor levels. Figure 3 reveals the
distribution of the random components of the data that determines the
repeatability characteristic of the robot. This graph indicates an
approximately normally distributed random pattern of error variation
about the mean for the particular factor level combination at which the

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THE TEXAS JOURNAL OF SCIENCE— VOL. 56, NO. 2, 2004

Residuals (.0001 inch)

Figure 3. Histogram of Residuals Errors. Residual errors were calculated by subtracting
the predicted radial error or accuracy from each measured radial error.

readings were taken. The computations in the analysis of variance
( ANOVA ) and the linear regression yielded the following equation to
predict the accuracy:

RMEAN(W,S,A) = 11.8 - 3.25 S + 1.44 A + 1.85 W - 3.32 W*?

- 3.02 W*A + 4.85 S*A + 2.23 W2 + 8.59 S2 + 4.21 A2
Where: W = weight, S = speed and A = percent of axis movement.

The computations confirmed that the three factors, as well as their
interactions, are statistically significant (P < 0.05) in the mean of the
radial error values. Analysis of variance (ANOVA) computations
produced a computed value of 98.4 for the variance of the random
component of the radial error values. The square root of the variance
yields the standard deviation of the random component to be 9.9. The
repeatability of a robot was defined to be three times the standard
deviation of the random component of the radial error. Therefore, the
estimate for the repeatability of the Puma 560 turns out to be 29.7.
Since measurements were in 0.0001 inch units, the repeatability estimate
would be stated as 0.00297 inch. The estimate is somewhat smaller than
the ±0.004 inch specified by the manufacturer. If regression techniques
had not been used to remove the variability due to the changes in the
factor levels, the standard deviation of the raw data would be 12.12.
This standard deviation yields 0.001212 when the units are changed to

BRINKS, HINDS & HANEY

155

inches and a corresponding repeatability estimate of 0.0036 inch. When
rounded to the nearest thousandth of an inch, this estimate agrees with
the manufacturer’s estimate.

The adequacy of such a model is usually judged by R 2, the coefficient
of determination, because it gives the fraction of the total variation in the
radial error data explained by the model. This model developed for
predicting the accuracy of the robot had an F? value of 35.2%. The
statistical analysis clearly indicates that all three factors, as well as their
interactions, affect the accuracy of the robot. However, the relationship
between these factors and the accuracy is such that the standard linear
regression techniques will not produce models which account for more
than approximately 35% of the radial error variability, leaving approxi¬
mately 65% of the radial error variability due to repeatability. When
using a robot, the accuracy of the robot at a particular setting of the
parameters can be determined by the regression model and adjustments
can be made to compensate for the predicted mean radial error. How¬
ever, the portion of the radial error which is due to repeatability must
be tolerated without recourse. Manufacturers should therefore concen¬
trate on giving more information about the accuracy of a robot. Since
they have extensive test data for each model of robot, the manufacturer
could provide a linear model for the purposes of predicting accuracy of
the robot as well as an estimate of the constant repeatability.

Acknowledgments

We thank the administration of Midwestern State University and
especially Dr. Norman Horner in providing the funds to perform this
research. We further like to thank Mr. Andy Webb for the construction
of the table and the testing fixture. We also thank Mrs. Lois Moore and
Dr. Michael Shipley for their advice. This paper would not have been
possible without the help of all these people and MSU institutional
support.

Literature Cited

ANSI. 1992. American National Standard for Industrial Robots and Robot Systems-
Path-Related and Dynamic Performance Characteristics-Evaluation-ANSI/RIA 15.05-2-
1992. American National Standards Institute, New York, 45 pp.

DeGarmo, P., J. T. Black & R. Kohser. 1997. Materials and Processes in Manufacturing,
8th ed. Prentice Hall, Upper Saddle River, New Jersey, 1259 pp.

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Khouja M. J. & R. L. Kumar. 1999. An options view of robot performance in a dynamic
environment. Int. J. Prod Res., 37 (6): 1244-1250.

Offodile, F. & K. Ugwu. 1991. Evaluating the effect of Speed and Payload on Robot
Repeatability. Robot. Comput.-Integr. Manuf., 8(l):27-28.

Rehg, J. 1985. Introduction to Robotics: A Systems Approach. Prentice Hall, Inc.,
Englewood Cliffs, New Jersey, 230 pp.

Warnecke, H. J. & R. D. Schraft. 1982. Industrial Robots, Application Experience. I.F.S.
Publications Ltd., Kempston, Bedford, England, 298 pp.

JB at: jan.brink@mwsu.edu

TEXAS J. SCI. 56(2): 157-170

MAY, 2004

HISTORICAL POPULATION DYNAMICS OF
RED SNAPPER (LUTJANUS CAMPECHANUS) IN THE
NORTHERN GULF OF MEXICO

J. R. Gold and C. P. Burridge

Center for Biosystematics and Biodiversity
Texas A&M University, College Station, Texas 77843-2258

Abstract.— A total of 313 young-of-the-year red snapper {Lutjanus campechanus )
belonging to the 1999 year class were sampled from three geographic regions in the northern
Gulf of Mexico and assayed for haplotype variation in mitochondrial (mt)DNA. Analysis
of molecular variance revealed that only a small proportion (0.24%) of the genetic variance
was distributed among regions; accordingly, the corresponding dPST value did not differ
significantly from zero. Exact tests of homogeneity of haplotype distributions also were
non-significant. Tests for departure from a neutral Wright-Fisher model of genetic
polymorphism, however, were significant, and a ‘mismatch’ distribution of nucleotide-site
differences in mtDNA indicated that the departure from neutrality could be due to population
expansion. Estimates of the time since expansion ranged from ==270,000 to =420,000 years
before present. The latter is consistent with the hypothesis that red snapper likely colonized
the continental shelf in the northern Gulf following a glacial retreat. The observed departure
from a neutral Wright-Fisher model also may suggest that insufficient time has lapsed for red
snapper in the northern Gulf to attain equilibrium between mutation and genetic drift.
However, the temporal signature provided by the ‘mismatch’ distribution is far older than
the last glacial retreat which began = 18,000 years ago. If the departure from neutrality
reflects events occurring after the last glacial retreat, tests of present-day population or stock
structure may well be compromised. The same may be true for other marine fish species in
the northern Gulf.

Red snapper ( Lutjanus campechanus) is an important, highly exploited
marine fish distributed primarily along the continental shelf in the Gulf
of Mexico from the Yucatan Peninsula in Mexico to the northeastern
Florida coast (Hoese & Moore 1998). Although the species has pro¬
vided an important fishery since the early 1900s, red snapper in U.S.
waters have declined by an estimated 90% since the 1970s (Goodyear
& Phares 1990). Factors impacting red snapper abundance include
overexploitation by directed commercial and recreational fisheries,
juvenile mortality associated with bycatch in the shrimp fishery, and
habitat change (Gallaway et al. 1999; Ortiz et al. 2000). Management
of red snapper resources in U.S. waters is currently based on a unit
stock hypothesis (GMFMC 1989). Whether red snapper in fact com¬
prise a single stock across the northern Gulf, however, remains an issue.
Separate management of regional stocks, if they exist, would be a de¬
sirable goal to avoid regional over-exploitation and to conserve adaptive
genetic variation (Carvalho & Hauser 1995; Hauser & Ward 1998).

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THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 2, 2004

Previous genetic work generally has been consistent with the existence
of a single stock of red snapper in the northern Gulf (Camper et al.
1993; Gold et al. 2001) and with the hypothesis that significant gene
flow occurs at one or more life-history stages (Goodyear 1995; Gold &
Richardson 1998a). The hypothesis of significant gene flow is not
consistent with a number of tagging studies that have shown adult red
snapper to be sedentary and exhibit high site fidelity (Szedlmayer &
Shipp 1994; Szedlmayer 1997). However, Patterson et al. (2001)
recently documented extensive movement of adult red snapper in the
northeastern Gulf and suggested that movement of adults might be
sufficient to facilitate mixing across the northern Gulf. A second
hypothesis is that observed genetic homogeneity reflects historic rather
than contemporary gene flow, and that present-day red snapper could be
isolated yet have been in sufficient genetic contact in the past to remain
genetically indistinguishable (Camper et al. 1993; Gold & Richardson
1998a). In such situations, populations may not have reached equi¬
librium between mutation and genetic drift, and if so, would be expected
to depart from expectations of the neutral Wright- Fisher model of
genetic polymorphism (Fu 1997).

This study examined the alternate hypothesis by assessing patterns of
mitochondrial (mt)DNA variation among red snapper sampled from three
geographic regions in the northern Gulf and asking whether mtDNA
haplotype distributions deviated from those expected under mutation-drift
equilibrium. Populations that are expanding or declining typically are
not in mutation-drift equilibrium (Fu 1997), and in such situations may
leave a characteristic ‘mismatch’ distribution signature (Rogers &
Harpending 1992). Consequently, this study also examined the
‘mismatch’ distribution of nucleotide site differences in mtDNA between
pairs of individuals in order to assess whether red snapper in the
northern Gulf had expanded or declined demographically. Red snapper
were likely precluded from occupying most of the contemporary
continental shelf in the northern Gulf during Pleistocene glacial advance
(Gold & Richardson 1998a), and colonization of shelf waters following
glacial retreat could have generated conditions conducive to population
expansion.

Materials and Methods

Young-of-the-year red snapper were procured in the fall of 1999
during a demersal trawl survey of the northern Gulf carried out by the

GOLD & BURRIDGE

159

National Marine Fisheries Service (NMFS). Individual fish were
sampled from the catch of a 12 m shrimp-trawl net, frozen onboard and
returned to College Station where tissues were removed and stored at
-80°C. Specimens were obtained from different offshore localities
corresponding to three geographic regions (Fig. 1) representing the
northwestern Gulf (south Texas coast, 14 trawls, n = 127, range/trawl
= 4-12, mode = 8), the northcentral Gulf (Louisiana coast, 14 trawls,
n = 123, range/trawl = 1-20, mode = 10), and the northeastern Gulf
(Mississippi- Alabama coast, 9 trawls, n = 63, range/trawl = 1-13,
mode = 10). Genomic DNA was isolated from frozen tissues as
described in Gold & Richardson (1991).

Assay of mtDNA employed single strand conformational
polymorphism or SSCP (Orita et al. 1989). Regions within the
NADH-4 (ND-4) and NADH-6 (ND-6) protein-coding genes were
sequenced and the Lasergene software package Primer Select was used
to design polymerase-chain-reaction (PCR) primers that amplified
mtDNA fragments less than 250 base pairs (bp) in size. The fragments
were 163 bp from ND-4 and 122 bp from ND-6. PCR primers (forward
primer first, then reverse primer) were as follows: ND-4 (5’ -
CAAAACCTTAATCTTCTACAATGCT - 3’; 5’ - CAGGGGGTCTGTTGCTAT -
3’) and ND-6 (5’ - CGAAGCGTCCCCCGACT - 3’; 5’ -

CGGTTGATGAACTAGGTGATTTTTC - 3’). PCR conditions followed those
used for red snapper microsatellites (Gold et al. 2001), except that
annealing was carried out at 58 °C and both primers for each fragment
amplified were radioactively labelled. Following PCR, 5/xL of stop
solution (95% formamide, 0.05% bromophenol blue and xylene cyanol,
10 mM NaOH) was added to 10/xL of PCR product. This solution was
heat denatured at 100° C for 10 min and then snap-chilled in ice water.
Varying gel composition and electrophoresis conditions optimized
resolution of electromorphs. Adequate resolution was provided by
electrophoresing PCR products at 500 V for 16 h on 8% non-denaturing
polyacrylamide gels (37.5:1 acrylamide: bis- acrylamide, 0.5X TBE),
supplemented with 5.0% glycerol (4.0% for NADH6) and run in 0.5X
TBE buffer. The ND-4 and ND-6 electromorphs were best resolved by
electrophoresis at 12 °C. Efficiency of SSCP procedures to identify
sequence variants was assessed by sequencing multiple representatives
of each electromorph and comparing patterns of sequence divergence
among them. Representatives of each electromorph were run on
subsequent SSCP gels as reference controls.

160

THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 2, 2004

Figure 1 . Collection localities of young-of-the-year red snapper ( Lutjanus campechanus)
from the northern Gulf of Mexico: northwestern Gulf {n = 127), northcentral Gulf ( n =
123, and northeastern Gulf ( n = 63).

MtDNA haplotype (nucleon) and nucleotide diversity were estimated
after Nei (1987). The former represents the probability that any two
individuals drawn at random will differ in mtDNA haplotype, whereas
the latter represents the number of nucleotide differences per site
between two randomly chosen sequences. Private haplotypes were
tabulated and a V test (DeSalle et al. 1987) was used to test whether the
proportion of private haplotypes differed significantly among regional
samples. Homogeneity of mtDNA haplotype distributions among
regions was assessed via analysis of molecular variance and exact tests
(based on a Markov-chain procedure). For Amova, significance of the
variance among samples and of Osx was assessed by permutation (10,000
replicates). Both tests of homogeneity were carried out using Arlequin
(Schneider et al. 2000).

Deviation from mutation-drift equilibrium was assessed via Fu & Li’s
(1993) D* and F* and Fu’s (1997) Fs measures of selective neutrality.
Tests of significance of Fu and Li’s D* and F* and Fu’s Fs statistics
were performed using DNAsp (Rozas et al. 2003) and Arlequin,
respectively, and were based on 1,000 (£>* and F*) and 10,000 ( Fs )
randomizations. Mismatch-distribution analysis (Rogers & Harpending

GOLD & BURRIDGE

161

1992) was used to assess population expansion. As populations at
mutation-drift equilibrium are expected to have ragged mismatch
distributions (Rogers & Harpending 1992), the r measure of 4 ragged¬
ness ’ (Harpending 1994) was calculated using Arlequin; tests of r —
0 were carried out by parametric bootstrapping (10,000 replicates), also
using Arlequin.

Results

Twelve electromorphs (A-L) of the 163 bp ND-4 fragment and
fourteen electromorphs (A-N) of the 122 bp ND-6 fragment were
identified via SSCP. Sequences of all electromorphs may be found in
Table 1. All electromorphs of the ND-4 fragment differed by no more
than a single nucleotide substitution from the most common electro-
morph (designated ‘A’); for the ND-6 fragment, two electromorphs (‘F’
and ‘G’) differed by more than one nucleotide substitution from any
other electromorph. Multiple representatives of each electromorph (both
fragments) were sequenced but no variation within an electromorph type
was detected.

A total of 32 composite mtDNA haplotypes were identified (Table 2).
Haplotypes AA, BB, and AC were the most common, occurring at
frequencies within regions of >0.300 (AA), 0.190 - 0.331 (BB), and
0. 134 - 0.238 (AC). Twenty-one private haplotypes were observed; the
number of private haplotypes per regional locality was 8 (Texas), 10
(Louisiana), and 3 (Mississippi/ Alabama). None of the private alleles
occurred at a frequency greater than 0.017, and the proportion of private
haplotypes did not differ significantly among regions (V[2J = 0.657, P
> 0.05). Nucleon and nucleotide diversities among regions were 0.770
(Texas), 0.776 (Louisiana), and 0.798 (Mississippi/ Alabama), and 0.006
(Texas), 0.007 (Louisiana), and 0.006 (Mississippi/ Alabama), respec¬
tively.

Analysis of molecular variance revealed that only 0.24% of the
molecular variation was distributed among samples rather than within
samples; the <4?ST value of 0.002 did not differ significantly ( P = 0.253)
from zero. An exact test of homogeneity in mtDNA haplotype distri¬
bution among regions also was non- significant ( P = 0.307). Given the
absence of heterogeneity in the distribution of mtDNA haplotypes among
samples, all mtDNA haplotypes were pooled into a single sample for all
subsequent analysis.

162

THE TEXAS JOURNAL OF SCIENCE— VOL. 56, NO. 2, 2004

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164

THE TEXAS JOURNAL OF SCIENCE- VOL. 56, NO. 2, 2004

Table 2. Frequencies of mitochondrial (mt)DNA haplotypes from age 0-1 red snapper
( Lutjanus campechanus ) sampled from three regions in the northern Gulf of Mexico.
Sample region and number of individuals are northwestern Gulf (TX, n '= 127),
northcentral Gulf (LA, n = 123), and northeastern Gulf (MS-AL, n = 63). First letter
(A-L) represents sequence eletromorphs at ND-4; second letter (A-N) represents sequence
electromorphs at ND-6. Electromorph sequences may be found in Table 1.

MtDNA

haplotype

MS-AL

MtDNA

haplotype

MS-AL

0.306

0.328

0.333

0.008

0.331

0.319

0.190

0.008

0.165

0.134

0.238

0.008

0.066

0.017

0.079

0.008

0.017

0.048

0.008

0.017

0.032

0.008

0.016

0.017

0.016

0.008

0.017

0.016

0.008

0.016

0.008

0.016

0.008

0.016

0.008

0.016

0.008

0.017

0.008

0.017

0.008

0.016

Fu & Li’s (1993) D* and F* and Fu’s (1997) Fs measures of selective
neutrality were negative and significant for the pooled samples (D* —
-2.85, P = 0.019; F* = -2.73, P = 0.007; Fs = -22.59, P = 0.000),
consistent with demographic growth of a population (Fu 1997). Popula¬
tion growth (expansion) also was indicated by the unimodal mismatch
distribution (Fig. 2) and by Harpending’s (1994) raggedness index (r)
which was non-significant (r = 0.107, P = 0.070). The time at which
demographic expansion in red snapper might have occurred was
estimated via the relationship r = 2ut (Rogers & Harpending 1992).
The value r is the crest or peak of a unimodal mismatch distribution
(measured in units of 1 Hu generations) , u is the mutation rate/generation
of the region under study, and t is time in generations. The estimate of
r (2.412) was obtained from Arlequin; u was estimated as the product
of trijjx , where mT is the number of nucleotides assayed (285) and fx is
an estimate of the mutation rate per nucleotide. For estimate(s) of /x, the
molecular-clock calibrations for mitochondrial protein-coding genes
developed by Bermingham et al. (1997) were used and employed two
rates (1.0% /106 yr and 1.5%/106 yr) for the (combined) ND-4 and ND-6
sequences from red snapper. For generation time, 15 and 20 years were
used, framing the hypothesized generation time in red snapper of 17-19
years (J. Cowan, Louisiana State University, pers. comm.). Estimates

GOLD & BURRIDGE

165

Figure 2. Mismatch distribution observed for mitochondrial DNA sequences (haplotypes)
of young-of-the-year red snapper ( Lutjanus campechanus ) from the northern Gulf of
Mexico. Bars represent observed frequency of differences between sequences; line
represents the expected distribution assuming demographic expansion.

of u ranged from 1.5 x 10'7/generation (/x = 1 . 0 % / 1 06 yr, 15 yr/
generation) to 3.0 x 107/generation (/x = 1 . 5 % / 1 06 yr, 20 yr/
generation). Estimates of the time when demographic expansion in red
snapper could have occurred ranged from « 200,000 yr (u = 3.0 x
107/generation) to — 540,000 yr (w = 1.5 x 107/generation). Despite
uncertainties surrounding appropriateness of the molecular clock
calibrations (Martin & Palumbi 1993; Rand 1994), and issues with use
of pairwise-difference parameters such as r (Felsenstein 1992), estimates
of the time since demographic expansion in red snapper fit well within
the Pleistocene epoch.

Discussion

The observed homogeneity of mtDNA-SSCP haplotype frequencies
among sample localities is consistent with the hypothesis that red
snapper constitute a single stock in the northern Gulf. Similar findings
were reported by Camper et al. (1993) based on restriction-site analysis
of whole mtDNA and by Gold et al. (2001) based on analysis of micro¬
satellites. Because genetic homogeneity typically implies sufficient gene
flow to offset genetic divergence, continuous movement of red snapper
at various life-history stages has been hypothesized (Goodyear 1995;
Gold & Richardson 1998a; Patterson et al. 2001).

The significant departure of mtDNA variation from expectations of

166

THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 2, 2004

the neutral Wright-Fisher model of genetic polymorphism indicates that
red snapper in the northern Gulf have not attained equilibrium between
mutation and genetic drift. Moreover, the negative values for the
‘neutrality’ indices, particularly Fu’s (1997) Fs index, suggest that the
departure from neutrality stems from population growth. However, in
addition to population growth, the D* and F* indices of Fu and Li
(1993) and the Fs index of Fu (1997) also can signify either background
selection or genetic hitchhiking, respectively (Fu 1997). Neither seems
plausible in this case, in part because data are from mtDNA which is
inherited as a single gene and independently from all nuclear genes, and
in part because the mismatch distribution and Harpending’s (1994)
raggedness index were consistent with the hypothesis of historical
population expansion. In addition, because red snapper were precluded
from occupying much of the contemporary continental shelf in the Gulf
when sea levels during Pleistocene glaciations were at least 100 m lower
than they are today (CLIMAP 1976; Rezak et al. 1985), colonization of
shelf waters and opening of favourable habitat following glacial retreat
would be expected to generate conditions conducive to population
expansion. This scenario is consistent with the estimated time of
* 200,000 - 540,000 years ago, given that the Pleistocene Epoch began
approximately 1.8 million years ago (http://vulcan.wr.usgs.gov/
Glossary /geotimescale . html) .

Camper et al. (1993) and Gold et al. (2001) suggested that the genetic
homogeneity observed among present-day red snapper in the northern
Gulf might reflect historical rather than current gene flow. Briefly,
genetic homogeneity among putatively isolated, present-day populations
could be sustained provided there has been both insufficient time since
colonization of continental-shelf waters and sufficiently large effective
population sizes such that allele frequency differences arising via
mutation have not reached mutation-drift equilibrium. However, the
time since expansion indicated from the mismatch distribution
( — 200,000 - 450,000 years ago) would seem too long for genetic
divergence not to have arisen, assuming there has been no gene flow
among localities and that effective population sizes are even one-tenth
to one-hundredth of the current estimated census size of 7 - 20 million
individuals. Unfortunately, estimating approximately how long it would
take for genetic divergence to arise in this situation is problematic, given
the absence of estimates of the effective (female) size of red snapper
populations in the northern Gulf and the possibly unrealistic assumptions
that red snapper form ‘idealized’ populations that exhibit an infinite-

GOLD & BURRIDGE

167

island model of population structure. On the other hand, the last glacial
retreat and the (re)opening of the continental shelf in the northern Gulf
was only within the last 18,000 years (Rezak et al. 1985), a time period
that is potentially too short for genetic divergence to occur if effective
(female) sizes are only 1-2 orders of magnitude smaller than current
census size and particularly if there is periodic gene flow among (semi-)
isolated stocks.

There are a number of caveats to the above inferences. The first is
that immigration of rare, genetically distinct mtDNA haplotypes also
could generate negative D*, F*, and Fs values (Skibinski 2000). How¬
ever, such immigration would be expected to lead to multimodal
mismatch distributions (Marjoram & Donelley 1994), unlike the
unimodal distributions observed here. A second caveat is that declining
rather than expanding populations also can produce unimodal mismatch
distributions. However, the ‘wave’ of a unimodal distribution of a
declining population is expected to have an extremely steep leading
edge, often with several secondary peaks that have large values (Rogers
& Harpending 1992), a pattern not observed in the mismatch distribution
generated from mtDNA sequences. Finally, the tests of neutrality may
not necessarily measure the same temporal period as the mismatch
distribution. The latter indicated a period of population expansion that
occurred between —200,000 and 450,000 years ago, whereas the tests
of neutrality could reflect an expansion dating to the last glacial retreat.
At present, there is no way to distinguish among these alternatives.

Assuming red snapper in the northern Gulf deviate from mutation-
drift equilibrium because of demographic expansion following the last
glacial retreat, the question arises as to how prevalent are the same
genetic patterns and demographic histories in other marine fishes in the
northern Gulf. Grant & Bowen (1998) hypothesized that the combina¬
tion of high haplotype diversity and low nucleotide diversity for mtDNA
was indicative of a population bottleneck followed by rapid growth (their
Category 2), and assigned two species that are common in the northern
Gulf (red drum, Sciaenops ocellatus, and greater amberjack, Seriola
dumerili) to this category. They erroneously assigned red snapper to
Category 1 (low haplotype diversity and low nucleotide diversity) based
on an error in reading Table 3 in Camper et al. (1993). Given the range
of haplotype (0.770 - 0.798) and nucleotide (0.006 - 0.007) diversity
found here, red snapper clearly belong in Category 2. A review of the
literature reveals that many other fishes in the northern Gulf also appear

168

THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 2, 2004

to belong to Grant and Bowen’s Category 2: Gulf toadfish, Opsanus
beta (cf. A vise et al. 1987); Spanish sardine, Sardine lla aurita (cf.
Tringali & Wilson 1993); common snook, Centropomus undecimalis (cf.
Tringali & Bert 1996), and black drum, Pogonias chromis , spotted
seatrout, Cy noscion nebulosus , and king mackerel, Scomberomorus
cavalla (synopsized in Gold & Richardson 1998b). Analysis of selective
neutrality and of mismatch distributions of mtDNA datasets may
demonstrate that these species also have undergone demographic
expansions that could be dated approximately to changes in habitat
availability during or following Pleistocene glaciation. Consequently,
it may be that the (spatial) genetic homogeneity observed for many
fishes in the northern Gulf of Mexico owes more to historical than
contemporary gene flow, and that stocks meriting independent manage¬
ment may have gone unnoticed. A final important point to note that
these current results do not necessarily reflect contemporary trends or
contradict the documented decline of present-day red snapper stocks
(Goodyear & Phares 1990), as evidence of historic demographic
expansion is not necessarily affected by even severe bottlenecks that
occur subsequent to population expansion (Rogers 1995; Lavery et al.
1996).

Acknowledgments

We thank W. Patterson for assistance in procuring samples, T.
Dowling for carrying out the V tests, and E. Saillant and T. Turner for
constructive comments on the manuscript. Research was supported by
a grant (NA87FF0426) from the MARFIN Program of the National
Marine Fisheries Service (Department of Commerce) and by the Texas
Agricultural Experiment Station under Project H-6703 . Views expressed
in the paper are those of the authors and do not necessarily reflect the
views of the sponsoring grant agencies. This paper is number 41 in the
series ‘Genetic Studies in Marine Fishes’ and Contribution 124 of the
Center for Biosystematics and Biodiversity at Texas A&M University.

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TEXAS J. SCI. 56(2), MAY, 2004

171

GENERAL NOTES

NOTES ON REPRODUCTION IN THE FALSE CORAL SNAKES,

ERYTHROLAMPRUS BIZONA AND ERYTHROLAMPRUS MIMUS
(SERPENTES: COLUBRIDAE) FROM COSTA RICA

Stephen R. Goldberg

Department of Biology, Whittier College
Whittier, California 90608

Erythrolamprus bizona ranges from Costa Rica, south to Colombia
and northern Venezuela and occurs from 8-1450 m in Costa Rica;
Erythrolamprus mimus ranges from Honduras through Panama, western
Colombia, Ecuador and northwestern Venezuela and occurs from 1-1200
m in Costa Rica (Savage 2002). Both are uncommon diurnal, secretive
snakes that are oviparous (Savage 2002) . The purpose of this note is to
provide information on reproduction from a histological examination of
gonadal material from museum specimens.

A sample of 40 specimens of E. bizona (females n = 25 , mean snout-
vent length [SVL] = 702 mm ± 83 SD , range = 545-835 mm; males
n = 15, SVL = 614 mm ± 54 SD, range = 535-715 mm) and a
sample of 13 specimens of E. mimus (females n = 7 , SVL = 557 mm
± 37 SD, range = 504-615 mm; males n = 6, SVL = 482 mm + 105
SD, range = 288-553 mm) from Costa Rica were examined from the
herpetology collection of the Natural History Museum of Los Angeles
County, Los Angeles (LACM). Erythrolamprus bizona were collected
1959-1980; E . mimus were collected 1966-1982. Counts were made of
enlarged ovarian follicles ( > 12 mm length) or oviductal eggs. The left
testis, vas deferens and a portion of the kidney were removed from
males and the left ovary was removed from females for histological
examination. Tissues were embedded in paraffin and sectioned at 5pm.
Slides were stained with Harris’ hematoxylin followed by eosin counter¬
stain. Histological slides were examined to determine the stage of the
testicular cycle and for the presence of yolk deposition (secondary
vitellogenesis sensu Aldridge 1979). Number of tissues histologically
examined by species were: E. bizona testis = 15, vas deferens = 15,
kidney = 15, ovary = 12; E . mimus testis = 6, vas deferens = 6,
kidney 6, ovary = 4. Follicles in advanced stages of yolk deposition or
oviductal eggs were counted, but not histologically examined. An
unpaired r-test was used to compare body sizes of male and female E.
bizona samples.

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THE TEXAS JOURNAL OF SCIENCE- VOL. 56, NO. 2, 2004

Material examined.— The following specimens of Ery thro lamp rus
bizona were examined by Costa Rica province: ALAJUELA (LACM
145932, 150656), CART AGO (LACM 145843, 145847, 145954, 147512,
150643, 150644, 150650-150653, 150657-150660, 150703, 150706-150708,
150710), GUANACASTE (LACM 150654), PUNT ARENAS (LACM 145792,
150704), SAN JOSE (LACM 67258, 145549, 145785, 145786, 145791,
145845, 145846, 145851, 145933, 145934, 145977, 147510, 150641, 150655,
150705, 150711). The following specimens of Ery thro lamp rus mimus
were examined by Costa Rica province: ALAJUELA (LACM 150714,
150715, 150723, 150725, 150728), HEREDIA (LACM 150716, 150717,
150719), LIMON (LACM 150720), PUNT AREN AS (LACM 150718,
150724), PROVINCE DATA MISSING (LACM 150721, 150722).

All testes examined from E. bizona and E. mimus were undergoing
spermiogenesis (= sperm formation) with metamorphosing spermatids
and sperm present. The following numbers of males were undergoing
spermiogenesis: E. bizona February (1), April (1), June (2), July (1),
August (1), September (1), October (5), November (1), December (2);
E. mimus March (3), October (1), December (1). One E. mimus male
(LACM 150728, SVL 288 mm) from February exhibited testicular recru¬
descence with spermatogonia and primary spermatocytes present. The
size at which this snake would have undergone spermiogenesis is un¬
known. All vasa deferentia contained sperm and all kidney sexual
segments from E. bizona and E. mimus were enlarged and contained
secretory granules. Mating usually coincides with enlargement of the
kidney sexual segments (Saint Girons 1982). The smallest E. bizona
male to undergo spermiogenesis (LACM 150659) measured 535 mm
SVL; the smallest E. mimus male to undergo spermiogenesis (LACM
150720) measured 432 mm SVL. It will be necessary to examine
additional males to ascertain the minimum sizes at which E. bizona and
E . mimus begin sperm formation.

Female E . bizona were significantly larger than males ( t = 3.67, df
= 38, P < 0.01). Samples of E. mimus were too small to make valid
size comparisons between males and females. Females of E. bizona
with oviductal eggs or enlarged follicles > 12 mm length were found
in January-March and September-November (Table 1). One female
from June (LACM 150650, SVL 111 mm) and one from October (LACM
150643, SVL 730 mm) were undergoing moderate yolk deposition and
contained follicles 5-6 mm in length. It was not possible to predict the
clutch size as other follicles might have undergone yolk deposition.
Three females were undergoing early yolk deposition (secondary vitello¬
genesis sensu Aldridge 1979): June (LACM 145785, SVL = 821 mm),

TEXAS J. SCI. 56(2), MAY, 2004

173

Table 1. Monthly distribution of stages in the seasonal ovarian cycle of Erythrolamprus
bizona from Costa Rica. Values shown are the numbers of females exhibiting each of the
five conditions.

Month

Inactive

Early yolk
deposition

Moderate yolk
deposition*

Enlarged follicles
> 12 mm length

Oviductal

eggs

January

February

March

May

June

July

September

October

November

December

*follicles 5-6 mm length; one cannot predict final clutch size.

September (LACM 150653, SVL = 720 mm), December (LACM 150707,
SVL = 645 mm). The smallest reproductively active female E. bizona
(LACM 145932) measured 602 mm SVL (Table 2). The minimum size
at which female E. bizona commence reproduction remains to be
determined. Clutch sizes are listed in Table 2. Mean clutch size for 1 1
E. bizona clutches was 5.5 ± 1.8 SD , range = 3-9.

Mean clutch size for 4 E. tnimus clutches was 3.8 ± 0.50 SD, range
= 3-4. Body sizes, collection dates and locations are in Table 2. The
smallest reproductively active female (oviductal eggs) measured 504 mm
SVL (Table 2). The minimum size at which E. mimus females begin
reproduction remains to be determined. One female from March
(LACM 150718, SVL = 615 mm) and one female from October (LACM
150722, SVL = 575 mm) were not undergoing yolk deposition. One
female E. mimus from December (LACM 150714, SVL = 563 mm)
was undergoing early yolk deposition (secondary yolk deposition sensu
Aldridge 1979).

There was no evidence that females of either E. bizona or E. mimus
produce more than one clutch per year (i.e., oviductal eggs and yolk
deposition in progress in the same female). However, in view of the
extended period in which males undergo spermiogenesis and reproduc¬
tively active females were found (Table 2), more than one clutch per
year might be possible. Erythrolamprus bizona deposits its eggs in
rotten logs or decomposed litter (Hardy & Boos 1995). Amaral (1978)
reported the congener Erythrolamprus aesculapii from Brazil produced
6-9 eggs. Marques (1996) reported reproduction occurred throughout
the year in E. aesculapii from southeastern Brazil and multiple clutches

174

THE TEXAS JOURNAL OF SCIENCE- VOL. 56, NO. 2, 2004

Table 2. Clutch sizes for Erythrolamprus bizona and E. mimus (estimated from counts of
enlarged follicles > 12 mm length or oviductal eggs*) from Costa Rica.

Date

SVL (mm)

Clutch size

Province

LACM #

3 January

827

Erythrolamprus bizona

Cartago

150651

24 January

760

Puntarenas

145792

26 January

670

San Jose

147510

27 January

700

Cartago

150708

1 February

835

San Jose

145549

16 February

783

San Jose

145786

16 March

667

San Jose

150641

2 September

650

San Jose

145845

12 October

695

Cartago

145847

17 October

750

Cartago

150706

24 November

602

Alajuela

145932

12 February

580

Erythrolamprus mimus

Alajuela

150715

8 March

533

Alajuela

150723

1 April

504

Puntarenas

150724

6 Sept

531

Heredia

150719

were recorded from captive snakes. Clutch sizes ranged from one to
eight eggs.

Additional monthly samples of E. bizona and E. mimus will need to
be examined to obtain further information on the reproductive biology
of these two species.

Acknowledgment

I thank D. A. Kizirian (LACM) for permission to examine specimens.

Literature Cited

Aldridge, R. D. 1979. Female reproductive cycles of the snakes Arizona elegans and
Crotalus viridis. Herpetologica, 35(3):256-261 .

Amarial, A. do. 1978. Serpentes do Brasil: iconografia colorida. Brazilian snakes: a color
iconography. 2nd Edit., Edit. Melhoramentos, Edit.Univ. Sao Paulo, Brasil, 246 pp.
Hardy, J. D., Jr., & H. A. E. Boos. 1995. Snakes of the genus Erythrolamprus (Serpentes:
Colubridae) from Trinidad and Tobago, West Indies. Bull. Maryland Herpetol. Soc.,
3 1 (3) : 158-190.

Marques, O. A. V. 1996. Biologia reprodutiva da cobra-coral Erythrolamprus aesculapii
Linnaeus (Colubridae), no sudeste do Brasil. Revta. Bras. Zool., 13(3):747-753.

Saint Girons, H. 1982. Reproductive cycles of male snakes and their relationships with
climate and female reproductive cycles. Herpetologica, 1 8(3) :5- 16.

Savage, J. M. 2002. The amphibians and reptiles of Costa Rica: A herpetofauna between
two continents, between two seas. Univ. Chicago Press, Chicago, Illinois, 934 pp.

SRG at: sgoldberg@whittier.edu

TEXAS J. SCI. 56(2), MAY, 2004

175

A NEW DISTRIBUTION RECORD AND NOTES ON
THE BIOLOGY OF THE BRITTLE STAR OPHIACTIS SIMPLEX
(ECHINODERMATA: OPHIUROIDEA) IN TEXAS

Ana Beardsley Christensen

Department of Biology, PO Box 10037
Lamar University, Beaumont, Texas 77710

Brittle stars (Echinodermata: Ophiuroidea) are a common component
of marine communities and often make up a significant portion of the
biomass. Identification, however, can be problematic, particularly in the
small fissiparous species. Fissiparity, asexual reproduction in which an
individual divides in two and regenerates missing parts, occurs in 34 of
the 2,000 species of brittle star (Emson & Wilkie 1980). One of these
is Ophiactis simplex, an eastern Pacific species, with distribution from
the Channel Islands to Panama and the Galapagos Islands (Neilsen 1932;
Lonhart & Tupen 2001). Like other fissiparous brittle stars most
specimens have six arms and are asymmetrical, with three long arms and
three shorter arms. However, individuals with Eve and seven arms are
not uncommon; the author has collected one with nine arms. One of the
distinguishing characteristics of this species is the red tube feet. The red
color is due to the presence of hemoglobin containing coelomocytes
(RBCs) present in the water vascular system (Christensen 1999).

In late May 2001, five specimens of O. simplex were collected in a
tide trap located on the research pier at the University of Texas Marine
Science Institute, in Port Aransas, Texas. The specimens were found
on algae caught in the net and were very small (disc diameter < 2 mm) .
Later that week approximately 200 specimens were collected from algae
and other fouling material scraped from the rocks of the south jetty at
Port Aransas. This represents a first report of this species along the
Texas coast. Official counts were not made at this time. Voucher
specimens were sent to Dr. Gordon Hendler at Museum of Natural
History of Los Angeles for positive identification. Several subsequent
collections have been made from the south jetty to determine habitat
preference and population structure.

In January 2002, various species of algae, sponge, hy droid and
tunicate colonies were scraped from the south jetty during an extremely
low tide. Brittle stars were removed from the substrate, counted, and
the volume of the substrate was estimated by measuring displacement

176

THE TEXAS JOURNAL OF SCIENCE— VOL. 56, NO. 2, 2004

volume. The brittle stars were sorted by disk diameter (large > 3 mm;
medium 2-3 mm; small < 2 mm), regeneration state (recently split [2
or more arms < 2 mm], regenerating [2 or more arms of unequal
length] and whole [all arms of equal length]) and redness of tube feet
(bright red, medium red and colorless). The redness of the tube feet is
a crude measure of the hematocrit (proportion of RBCs to water vascular
system fluid). It is noted that individual hematocrit is variable in the
Texas population: individuals possessing bright red tube feet have large
numbers of RBCs in the water vascular system while others have color¬
less tube feet due to the scarcity of RBCs in the water vascular system.
Actual hematocrits were not measured but were inferred from micro¬
scopic examination of several dissected individuals.

Collections were made again in June 2002, January and July 2003,
primarily from colonies of the tunicate Eudistoma carolinense .

The densest aggregations of Ophiactis simplex were found in colonies
of the sandy lobed tunicate, Eudistoma carolinense (75 individuals per
100 mL) (Table 1). Other substrates in which O. simplex were found
included fire sponge ( Tedania ignis), eroded sponge ( Haliclona
loosanoffi) and brown ribbed algae (. Dictyopteris sp.) (Table 1). In
January 2002, a total of 537 individuals was collected. Medium size
individuals (2-3 mm disc diameter) were dominant (67%) and 58% of
the individuals were nearly full or fully regenerated (Table 2). In
contrast, the June 2002 collection yielded 414 individuals, 70.8%
belonging to the small size class (< 2 mm disc diameter) and 82.6% of
the individuals were in some stage of regeneration (Table 2). These
animals were not sorted by tube feet color as significant mortality
occurred before sorting. In July 2003, 229 individuals were collected,
88.2% belonging to the small size category and 83.4% were in some
stage of regeneration.

Fission appears to be an important means of reproduction in the small
and medium size classes, as most collected were in some stage of
regeneration. Only two of the 27 large individuals collected were
regenerating. The large size class also appears to be fairly uncommon;
the largest individual collected had a disc diameter of 4.8 mm. Sexual
reproduction also plays a role in this population of O. simplex. In the
June 2002 collection, a large proportion (186 individuals) of the small
size class was < 1 mm. The high number of small individuals indicates
larval recruitment into the area (Mladenov & Emson 1984). Although

TEXAS J. SCI. 56(2), MAY, 2004

177

Table 1. List of substrates and densities from which Ophiactis simplex was collected. The
different numbers associated with Eudistoma carolinense represent different colonies of
the tunicate.

Species

Density

Tedania ignis

15/100 mL

Haliclona loosanoffi

17/100 mL

Dictyopteris sp.

8/100 mL

Eudistoma

35/100 mL

Eudistoma #2

41/100 mL

Eudistoma #3

79/100 mL

Eudistoma #4

28/100 mL

Eudistoma #5

61/100 mL

Eudistoma #6

25/100 mL

Table 2. Results of sorting the collections on the basis of size (small: disc diameter < 2 mm;
medium: disc diameter 2-3 mm; and large: disc diameter > 3 mm); regeneration state
(recently split: half disc and 2 or more arms < 2 mm; regenerating: 2 or more arms of
unequal length; and whole: all arms of equal length), and color of tube feet (indication
of hematocrit).

January, 2002 June, 2002 July, 2003

Size

Small
Medium
Large

Regeneration state

Recently split
Regenerating
Whole

Color of tube feet

Bright red
Medium red
Colorless

157

293

202

359

117

191

275

160

312

199

196

128

142

* June, 2002, sample not sorted for color of tube feet due to significant mortality before
sorting. The red color fades with death.

nothing has been reported on the reproductive periodicity of O. simplex ,
the appearance of so many extremely small individuals in the summer
suggests an early spring spawn period. The July 2003 sample also
yielded many very small animals but the exact numbers were not
quantified.

There does not appear to be any relationship between regeneration
state and color of tube feet. However, there does appear to be a weak
relationship between size and color. There was only one large indi-

178

THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 2, 2004

Figure 1. Aboral (surface) views of Ophiactis savignyii (left) and Ophiactis simplex (right).

vidual (disc diameter 3 mm) with colorless tube feet; all other large
individuals possessed either medium or bright red tube feet. The larger
individuals may be dependent upon hemoglobin for oxygen transport due
to their reduced surface area to volume ratio whereas smaller individuals
are likely small enough to obtain sufficient oxygen needed for aerobic
metabolism by simple diffusion. Differences in the numbers of RBCs
among individuals of the same size class may be due to oxygen availa¬
bility in the microhabitat: those with bright red tube feet may inhabit
areas with a lower oxygen tension than those with colorless tube feet.
This possibility will be investigated further.

It is not known if this population of O. simplex is a recent introduc¬
tion (e.g. , through ballast water or drift algae) or if it has been present,
but misidentified. A closely related species, Ophiactis savignyii , appears
on collection lists for the area. Both are small and fissiparous, but O.
savignyii does not possess hemoglobin. As mentioned earlier, not all
specimens of the Texas population possess large amounts of hemoglobin
and the red color disappears upon preservation with alcohol or formalin.
Even with the small size, the two species are morphologically different.
The radial shields (two at the base of each arm) of O. savignyii are very
large; the length often exceeds half the disc radius, while those of O.
simplex are much smaller (Hendler et al 1995) (Figure 1). The arm
spines are also markedly different: 4-5 long thin spines in O. simplex
and 5-6 shorter, stubby spines in O. savignyi.

Acknowledgments

I would like to thank the following: Dr. Gordon Hendler for the
morphological identification; Dr. David Hicks for his aid in collections;

TEXAS J. SCI. 56(2), MAY, 2004

179

Denise Dean for assistance in counting and sorting brittle stars; and Jay
Carroll at Tenera Environmental for collection of California O. simplex
for comparisons; Drs. Richard Harrel and Andy Kasner for their
comments on the manuscript.

Literature Cited

Christensen, A. B. 1998. The properties of the hemoglobins of Ophiactis simplex
(Echinodermata, Ophiuroidea). Am. Zool., 38:12.

Emson, R. H. & I. C. Wilkie. 1980. Fission and autotomy in echinoderms. Oceanogr.
Mar. Biol. Ann. Rev., 18: 155-250.

Hendler, G., J. E. Miller, D. L. Pawson & P. M. Kier. 1995. Sea stars, sea urchins, and
allies: Echinoderms of Florida and the Caribbean. Smithsonian Institution Press,
Washington. 390 pp.

Lonhart, S. I. & J. W. Tupen. 2001. New range records of 12 marine invertebrates: The
role of El Nino. Bull. Southern California Acad. Sci., 100:238-248.

Mladenov, P. V. & R. H. Emson. 1984. Divide and broadcast: sexual reproduction in the
West Indian brittle star Ophiocomella ophiactoides and its relationship to fissiaprity.
Mar. Biol., 81:273-282.

Nielsen, E. 1932. Ophiurans from the Gulf of Panama, California, and the Strait of
Georgia. Vidensk. Medd. fra Dansk naturh. Foren., 91: 241-346 [pp. 257-60].

ABC at: christenab@hal.lamar.edu

5)« * *

FIRST DEFINITIVE RECORD OF MORE THAN
TWO NESTING ATTEMPTS BY WILD WHITE- WINGED DOVES
IN A SINGLE BREEDING SEASON

Cynthia L. Schaefer, Michael F. Small, John T. Baccus
and Roy D. Welch*

Department of Biology, Texas State University -San Marcos
San Marcos, Texas 78666 and
*Texas Parks and Wildlife Department, 1601 East Crest Drive
Waco, Texas 76705

The historical breeding range and recruitment of white-winged doves
( Zenaida asiatica) in Texas was primarily restricted to a four-county
region in the lower Rio Grande Valley (Cottam & Trefethen 1968).
Recruitment in peripheral populations in adjacent south Texas counties
and the Trans-Pecos region have been considered negligible (Gray
2002). In recent years, white- winged dove nesting chronology data have
shown a geographic shift in nesting to include urban areas (Small &
Waggerman 2000). This shift in nesting range occurred concurrent with

180

THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 2, 2004

a substantial northward range expansion of breeding white-winged
doves, colonization of urban areas, and establishment of year-round
populations over the last three decades (George et al. 1997; Schwertner
et al. 2002).

As white- winged doves continue expanding their range and congregat¬
ing in urban habitats, accurate measurement of annual recruitment is
fundamental to understanding the ecology of this dynamic species.
White-winged doves can nest twice in a single breeding season with
speculation by some biologists of a greater number of nesting attempts
(Cottam & Trefethen 1968, Alamia 1970, Swanson 1989). However,
definitive records of more than two nesting attempts have not been
documented prior to our account.

Two studies of breeding white- winged doves were conducted using
surgically implanted radio transmitters. In 2000, breeding white- winged
doves were monitored in Kingsville, Texas and in 2002-2003 in Waco,
Texas. All white- winged doves were trapped locally in standard wire
funnel traps (Reeves 1968) and implanted with subcutaneous radio
transmitters in the field at trap sites (Small et al. 2004). In 2000, 40
doves (24 males, 16 females) were trapped and implanted between 19
May and 9 June. All doves were located to source once/ week until
onset of nesting. Nests were then monitored every four days using a
mirror on an extendable pole and nest status recorded.

In 2002, 39 doves (16 males, 23 females) were trapped and implanted
with transmitters in June and in 2003, 40 doves (17 males, 16 females,
six unknown) were trapped and implanted in February and March. All
doves were monitored as in 2000, for the life of the transmitter, up to
but not exceeding 90 days.

During 2000, three male white- winged doves participated in three
nesting attempts with unmarked females. Each attempt resulted in new
nest construction. In each case, two nesting attempts proved successful
with 1 failure. Young fledged on the first and second nesting but failed
on the third for two nesting pairs. The other fledged young on the first
and third attempts with the second failing. During 2002, one white¬
winged dove (sex unknown) made three nesting attempts. Two attempts
fledged young, nests 1 and 2, with nest 3 failing. During 2003, one
female white-winged dove made four nesting attempts with the first and
fourth attempts fledging young. The second attempt resulted in nest

TEXAS J. SCI. 56(2), MAY, 2004

181

Table 1. Observations for an individual white-winged dove attempting four successive
nestings.

Nest

Tree

Attempt

Date

Success

Height

(m)

Distance
from
last nest
(m)

Species

Height

(m)

Same/

Different

04/08/03

2 fledged

2.32

Pecan

6.67

05/23/03

abandoned

2.90

7.0

Pecan

6.67

same

06/11/03

nest failed

8.06

7.0

Live Oak

16.64

different

06/18/03

2 fledged

2.33

7.0

Pecan

6.67

different

abandonment and the third nest failed.

In all multiple nesting attempts, no doves reused a nest. Doves built
new nests either in the same tree or a nearby tree = 100 m from the old
nest. Because of its uniqueness, additional information for the individual
with four nesting attempts is presented (Table 1).

Although some anecdotal evidence of > two nesting attempts by
white- winged doves exists, radio telemetric methodology allowed us to
report the first definitive occurrence of > two nesting attempts.
Whether this is a unique occurrence or a fundamental aspect of
white- winged dove natural history is unknown. Because of the dynamic
range expansion, urbanization, and proportional residency shifts of
white- winged doves over the last 30 - 50 years, frequency of > two
nesting attempts in historic populations will probably never be known.

The availability of anthropogenic food and water resources and habitat
associated with urbanization have the potential to extend the breeding
season (Hayslette & Hayslette 1999) which could represent a shift in the
reproductive strategy for white- winged doves. During 2002, one pair
of doves with radio transmitters pair bonded, but both batteries failed
after 1 successful nesting. Consequently, the issue of monogamy in wild
populations of white- winged doves remains unanswered in this study.
Further research is fundamental to understanding the dynamics of
multiple nesting, monogamy and an extended breeding season on
recruitment.

This report was part of a study funded by the Texas Parks and
Wildlife Department’s white-winged dove stamp research fund.

182

THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 2, 2004

Literature Cited

Alamia, L. A. 1970. Renesting activity and breeding biology of the white-winged dove
{Zenaida asiatica ) in the lower Rio Grande Valley of Texas. Unpubl. M.S. thesis, Texas
A&M University, College Station, Texas, USA, 126 pp.

Cottam, C. & J. B. Trefethen. 1968. Whitewings: the life history, status, and management
of the white-winged dove. D. Van Nostrand Inc., New York, New York, USA, 348 pp.
George, R. R., R. E. Tomlinson, R. W. Engel-Wilson, G. L. Waggerman, & A. G. Spratt.
1994. White-winged dove. Pages 28-50, in T. C. Tacha and C. E. Braun, editors.
Migratory shore and upland game bird management in North America, Allen Press,
Lawrence, Kansas, USA, 223 pp.

Gray, M. G. 2002. Breeding biology of White- winged Doves {Zenaida asiatica ) with
subcutaneously implanted transmitters in Kingsville, Texas. Unpubl. M.S. thesis.
Southwest Texas State University, San Marcos, Texas. 51 pp.

Hayslette, S. E. & B. E. Hayslette. 1999. Late and early season reproduction of urban
white-winged doves in southern Texas. Texas Journal of Science, 51 (2): 173-180.
Reeves, H. M., A. D. Geis, & F. C. Kniffin. 1968. Mourning dove capture and banding.
United States Fish and Wildlife Service, Special Scientific Report 117, Washington, D.
C., USA, 63 pp.

Schwertner, T. W., H. A. Mathewson, J. A. Roberson, M. Small, & G. L. Waggerman.
2002. White-winged Dove {Zenaida asiatica), in A. Poole & F. Gill, editors. The Birds
of North America, No. 710. The Birds of North America, Inc., Philadelphia,
Pennsylvania, USA, 28 pp.

Small, M. F. & G. L. Waggerman. 1999. Geographic redistribution of breeding
white-winged doves in the lower Rio Grande Valley of Texas: 1976-1997. Texas Journal
of Science, 51(1): 15-19.

Small, M. F., J. T. Baccus & G. L. Waggerman. 2004. Mobile anesthesia unit for
implanting radio transmitters in birds in the field. The Southwestern Naturalist,
49(2): 279-282.

Swanson, D. A. 1989. Breeding biology of the white- winged dove {Zenaida asiatica) in
south Texas. Unpubl. M.S. thesis, Texas A&I University, Kingsville, Texas, USA, 121

pp.

SLS at: cyndyschaefer@yahoo.com

THE TEXAS JOURNAL OF SCIENCE— VOL. 56, NO. 2, 2004

183

Plan Now for the
108th Annual Meeting of the
Texas Academy of Science

March 3 - 5, 2005
University of Texas-Pan American

Local Host

Program Chair
Damon Waitt

Lady Bird Johnson Wildflower Center
4801 LaCrosse Ave.

Austin, Texas 78739
Phone: 512.292.4200
E-mail: dwaitt@wildflower.org

Hudson DeYoe
Dept, of Biology and
Center for Subtropical Studies
University of Texas-Pan American
1201 West University Dr.
Edinburg, Texas 78541
Phone: 956.381.3538
FAX: 956.381.3657
E-mail: hdeyoe@panam.edu

For additional information relative to the Annual Meeting,
please access the Academy homepage at:

www . texasacademyofscience.org

Future Academy Meetings

2006 - Lamar University

2007 - Baylor University

THE TEXAS ACADEMY OF SCIENCE

www.texasacademyofscience.org

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Volume 56
Number 3
August 2004

GENERAL INFORMATION

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THE TEXAS JOURNAL OF SCIENCE

Volume 56, No. 3

August, 2004

CONTENTS

Observations of Bird Communities in Relation to Reservoir Impoundment.

By Dean Ransom, Jr. and R. Douglas Slack . 187

Seasonal and Ecological Associations of the Avifauna from
Sierra San Antonio-Pena Nevada, Zaragoza, Nuevo Leon, Mexico.

By Irene Ruvalcaba- Ortega, Jose I. Gonzalez-Rojas,

Armando J. Contreras-Balderas and Alina Olalla-Kerstupp . 197

Mate Guarding in Northern Mockingbirds {Mimus polyglottos).

By Rebecca Y. Bodily and Diane L. H. Neudorf . 207

A Late Cretaceous Durophagus Shark, Ptychodus martini Williston,
from Texas.

By Shawn A. Hamm and Kenshu Shimada . 215

New Records of the Texas Homshell Popenaias popeii (Bivalvia: Unionidae)
from Texas and Northern Mexico.

By Ned E. Strenth, Robert G. Howells and Alfonso Correa-Sandoval . 223

Paraboloids for Maximum Solar Energy Collection.

By Ali R. Amir-Moez . 231

Characteristics of Peripheral Populations of Parthenogenetic
Cnemidophorus laredoensis A (Squamata: Teiidae), in Southern Texas.

By James M. Walker, James E. Cordes and Mark A. Paulissen . 237

Comparison of Branch Elongation among Four Acacia Species and Texas Ebony

in the Lower Rio Grande Valley of Texas.

By Melissa R. Eddy and Frank W. Judd . 253

general Notes

Systematic and Ecological Notes on Tubificoides heterochaetus
(Oligochaeta: Tubificidae) from the Neches River Estuary, Texas.

By Richard C. Harrel . 263

Reproduction in the Western Hognose Snake, Heterodon nasicus
(Serpentes: Colubridae) from the Southwestern Part of its Range.

By Stephen R. Goldberg . 267

Endoparasites of the Sequoyah Slimy Salamander, Plethodon sequoyah
(Caudata: Plethodontidae), from McCurtain County, Oklahoma.

By Chris T. McAllister and Charles R. Bursey . 273

Annual Meeting Notice for 2005 . 278

Recognition of Member Support . . . . . . . 279

Membership Application . 280

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Associate Editor for Environmental Science:

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American Association for the Advancement of Science,

TEXAS J. SCI. 56(3): 187-196

AUGUST, 2004

OBSERVATIONS OF BIRD COMMUNITIES
IN RELATION TO RESERVOIR IMPOUNDMENT

Dean Ransom, Jr. and R. Douglas Slack

Texas A&M University Agricultural Experiment Station
P. O. Box 1658, Vernon, Texas 76384 and
Department of Wildlife and Fisheries Sciences, 210 Nagle Hall
Texas A&M University, College Station, Texas 778433-2258

Abstract.— This study describes trends in terrestrial avian communities in response to
construction of Aquilla Lake in north-central Texas. Reservoir construction and filling
resulted in substantial loss of area in each of four major habitat types. Pre-impoundment
surveys began in 1979, with follow up post-impoundment surveys in 1984, 1987 and 1992.
Mean bird density, species richness and species diversity were highest among all seasons
during the pre-impoundment survey, but declined markedly by the first post-impoundment
study. Similarity in bird species composition was greatest among the post-impoundment
avian communities. Northern cardinal ( Cardinalis cardinalis ) and Carolina chickadee
( Poecile carolinensis ) were the two most common species encountered in all seasons across
study phases. Comparisons with data from two adjacent North American Breeding Bird
Survey routes suggest that declines among six species may have been related to reservoir
construction. Over time, post-impoundment bird communities on Aquilla Lake had fewer
bird numbers, had fewer bird species, and were more similar to one another in species
composition.

Riparian habitats are productive, diverse and structurally complex
habitats that support large aggregations of breeding and riparian
dependent bird species (Carothers & Johnson 1975). These habitats also
provide critical resources to more vertebrate species than any other
habitat type, yet less than 2% of the United States (US) land area is
comprised of this habitat type (Sedgwick & Knopf 1987; Douglas et al.
1992; Naiman et al. 1993). Further, > 89% of riparian habitat in the
US has been lost over the last 200 years, primarily due to logging,
agricultural practices and development (Douglas et al. 1992; Croonquist
& Brooks 1993). The damming of stream and river systems for reser¬
voir construction has also resulted in substantial loss of riparian habitats.

Reservoirs are created for a variety of uses that include flood control,
recreation and municipal water supply. As human populations continue
to grow, the demand for water resources will continue to increase with
greater emphasis on reservoir construction to supply that need. In
Texas, for example, there are currently 440 reservoirs with greater than
400 ha of conservation storage capacity; 211 of these have greater than
2,000 ha of conservation storage capacity (Texas Water Development

188

THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 3, 2004

Board 2002). Construction of an additional eight major and 10 minor
reservoirs has been recommended to meet the future water needs of a
growing Texas population beyond 2002, as mandated by the state water
plan (Texas Water Development Board 2002). Also, 33 sites uniquely
suited for reservoir development have been identified for future
development by water board planning groups. Reservoir construction
can have negative impacts on habitat for terrestrial wildlife species.
Impoundment of natural watercourses results in direct loss of species-
rich riparian habitats, and fragmentation of remaining forest patches.
The proposed construction of 44 reservoirs in Texas during the early
1990s, for example, would have directly impacted an estimated 344,399
ha of wildlife habitat (Frye & Curtis 1990).

Habitat loss and fragmentation effects on terrestrial bird communities
have been well studied in numerous environments (Ambuel & Temple
1983; Terbourgh 1989; Hill & Hagen 1991; James et al. 1992; Sauer &
Droege 1992; Andren 1994; Herkert 1994; Winter & Faaborg 1999;
Coppedge et al. 2001). The impacts on terrestrial avian communities
resulting from construction and subsequent filling of reservoirs have
largely been ignored by avian ecologists. This is surprising in light of
the many reservoirs that exist throughout the southern US, and Texas in
particular. This study describes the changes in terrestrial avian com¬
munities in context to reservoir construction in north-central Texas over
a 14 year time frame.

Methods

Study area. — The project study site was located in Hill County,
approximately 1 1 .2 km southwest of Hillsboro, Texas. The project area
was defined as all lands purchased in fee and/or easement necessary for
reservoir construction, as well as all lands within the flood pool eleva¬
tion of 169.5 m. The 4,133.2 ha study site was located within the
Black-land Prairie and eastern Cross Timbers and Prairies vegetation
zones (Gould 1975; Slack et al. 1996). The Blackland Prairie region
has alkaline black clay soils with high organic content overlying parent
Cretaceous limestone. Prior to agricultural conversion, the dominant
herbaceous vegetation was little bluestem (Schizachrium scoparium );
currently it is confined to small scattered areas in the eastern part of the
county. The Eastern Cross Timbers consists of a belt of post oak
( Quercus stellata ) and blackjack oak ( Q> . marilandica) extending from
the Red River into southern Hill County. The terrain of the study site

RANSOM & SLACK

189

was nearly level to rolling, and was dissected by Aquilla, Little Aquilla
and Hackberry Creeks. Impoundment of Aquilla Lake by the U.S.
Army Corps of Engineers (USACOE) began on 29 April 1983 and
reached conservation pool level (163.9 m) two years later on 21 March
1985. The dam site was located in Hill County (97°13’24"W,
31°054’44"N) on Aquilla Creek at river mile 23.6 (km 38).

Habitat mapping and bird surveys. — Major habitat types within the
project boundaries were mapped and their post- impoundment areal
changes quantified from color aerial photographs using ARCINFO
Geographic Information System beginning with the pre- impoundment
phase I (1979), and each post- impoundment phase: II (1984), III (1987),
IV (1991). The avian community was surveyed using three 40 m wide
belt transects established prior to lake construction; transects were placed
in a manner that would sample the major habitat types in proximity to
the projected reservoir basin. Each transect differed in length and
sampled habitat types to varying degrees. Transect one was initially 3.7
km long, 37%, 53% and 9.9% of which was represented by forest
parkland, old field and riparian woodland habitat types, respectively.
Transect one was reduced in length by rising water levels to 2.8 km and
2.5 km in 1987 and 1984, respectively. Transect two was 2.8 km long,
97% of which was in the old field habitat type. Transect three was 1.7
km long and was comprised of 38% forest parkland, 16% riparian
woodland and 46% old field habitat. Lengths of transect two and three
were unaffected by the filling of the reservoir.

Initially, a transect was established in riparian woodland habitat off
the reservoir acquisition site as a control to evaluate reservoir impacts.
In the winter of 1984, this site was cleared and converted to tame
pasture, negating its use as a true control; results from this transect are
not reported in this study. To establish some context for interpreting
reservoir effects, data from two North American Breeding Bird Survey
(BBS) routes located near Aquilla Lake over the same time period (Sauer
et al. 2001) was compared. Abundance data for the 11 most abundant
species encountered during June surveys on Aquilla Lake were obtained
from the Osage BBS route (TEX-050, 97°33’27MW, 31°22’23nN) and
the Pidcoke BBS route (TEX-051, 97°52,29,,W, 31°20’29"N), pooled
(n = 27) and regressed against time (1979-1992). The hypothesis that
the slope of the regression line (fy) for each species did not differ using
95 % confidence intervals (Johnson 1999) was tested. If a particular bird
species declined on the study site post- impoundment and also was

190

THE TEXAS JOURNAL OF SCIENCE— VOL. 56, NO. 3, 2004

Table 1. Area (ha) and percent change (%) over time of habitat types on Aquilla Lake
reservoir site. Years correspond to pre-impoundment (1979-80), and post-impoundment
I (1984-85), II (1987-88) and III (1991-92) surveys.

Habitat Type

1979-80

1984-85

1987-88

1991-92

Forest Parkland

428.8

331.8

-22.6

235.3

-29.0

235.3

Scrub/Shrub

484.6

29.3

-93.9

25.2

-14.0

25.2

Riparian Woodland

1633.8

614.3

-62.4

57.2

-90.7

57.2

Old-field 1

735.5

660.4

-10.2

435.4

-34.0

435.4

1 Includes area of crop, pasture and old-field habitats pre-impoundment.

declining on BBS routes for the same time frame, this would suggest
that reservoir construction had little or no effect on the changing
numbers for that species.

Transects were walked once per quarter during the first three hours
of daylight. All birds seen within 20 m on either side of the transect
line were identified and recorded. Each of the post- impoundment
studies employed a different observer in conducting transect counts.
Bird density was calculated seasonally on each transect by dividing the
number of birds seen by the area covered (transect length x 40 m);
transect density estimates were averaged to obtain a mean bird density
(birds/ha ± SE) across the study area. Species richness (r), Simpson’s
D, Shannon’s diversity (H’) and Morisita’s index of similarity (Krebs
1989) were computed seasonally for pre-impoundment and post¬
impoundment surveys to compare seasonal bird communities across all
phases of this study.

Results

Four major habitat types were classified from pre- impoundment aerial
photographs: forest parkland, riparian woodland, scrub/shrub and old
field. All four habitats types were reduced in area due to reservoir
construction (Table 1). Riparian woodland was the largest habitat type
prior to impoundment and experienced the most rapid rate of loss over
the course of the study (Table 1).

Mean bird density and species richness was higher in the pre¬
impoundment phase across seasons than in all post-impoundment phases
(Table 2); pre- impoundment bird densities were highest during fall and
summer. Bird density then declined in all seasons (< 10 birds/ha)
between the pre- impoundment and the first post- impoundment phase

RANSOM & SLACK

191

Table 2. Species richness (r), Simpson’s D (S[D]) and Shannon-Weiner H’ (SW[H’])
diversity values, and mean density (D, birds/ha) and standard error (SE) for land-bird
communities by year and season on Aquilla Lake. Years correspond to pre-impoundment
(1979-80), and post-impoundment I (1984-85), II (1987-88) and III (1991-92) surveys.

Season

Year

S(D)

SW(H’)

D(SE)

Winter

1979-80

0.931

3.003

20.2

(6.1)

1984-85

0.914

2.731

8.7

(2.4)

1987-88

0.789

1.913

3.5

(0.9)

1991-92

0.870

2.269

5.3

(1.7)

Spring

1979-80

0.918

2.987

24.7

(5.4)

1984-85

0.858

2.252

6.3

(0.8)

1987-88

0.891

2.309

2.4

(0.8)

1991-92

0.915

2.504

2.8

(1.0)

Summer

1979-80

0.907

2.978

59.6

(9.8)

1984-85

0.872

2.187

2.2

(1.1)

1987-88

0.766

1.864

2.8

(0.5)

1991-92

0.840

2.226

2.9

(0.7)

Fall

1979-80

0.907

3.037

77.4

(19.6)

1984-85

0.851

2.137

2.8

(1.3)

1987-88

0.783

1.865

2.6

(0.8)

1991-92

0.868

2.113

2.1

(0.8)

(Table 2). Species richness values also declined >50% across seasons
between the pre- impoundment and first post-impoundment sampling
periods (Table 2); pre- impoundment richness values were highest during
winter and summer.

Morisita’s index of similarity revealed a reduction in similarity
between the pre- impoundment survey and all post- impoundment surveys
during the fall and winter seasons (Table 3). Collectively, post¬
impoundment bird communities were most similar to the pre-impound¬
ment values during the summer (Table 3). In all seasons but winter,
there was greater similarity among post-impoundment surveys than
between pre- impoundment and post- impoundment comparisons (Table
3). The similarity between pre- impoundment and post- impoundment
bird communities exceeded 50% only in the summer survey periods.

Forty-eight percent (n = 19), 51% (n = 23), 54% ( n — 23) and 79%
( n = 66) of the birds recorded during the pre- impoundment surveys
during winter, spring, summer and fall, respectively, were never
recorded in the subsequent post-impoundment surveys. The two most
abundant species encountered in all seasons and surveys were northern
cardinal and Carolina chickadees; American robins and eastern meadow¬
larks were most abundant during the winter and spring surveys.

192

THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 3, 2004

Table 3. Morisita’s community similarity values of seasonal pre-impoundment and
post-impoundment land bird communities over time on Aquilla Lake, Hill County, Texas.
Years correspond to pre-impoundment (1979-80), post-impoundment I (1984-85), II
(1987-88) and III (1991-92) surveys.

Season

Year

1984-85

1987-88

1991-92

Winter

1979-80

0.685

0.485

0.404

1984-85

0.631

0.255

1987-88

0.267

Spring

1979-80

0.332

0.385

0.339

1984-85

0.667

0.648

1987-88

0.674

Summer

1979-80

0.448

0.571

0.607

1984-85

0.829

0.858

1987-88

0.967

Fall

1979-80

0.310

0.269

0.224

1984-85

0.514

0.505

1987-88

0.843

Twenty-four species of neotropical migrants were observed during the
summer pre- impoundment phase of the study. Yellow-billed cuckoos
(Coccyzus americanus ) and dickcissels (, Spiza americana ) were the most
abundant neotropical migrants in all four phases of summer surveys, and
both exhibited the most marked decline in post- impoundment surveys.

The 1 1 most abundant birds seen during summer surveys on Aquilla
Lake included northern bob white ( Colinus virginianus) , northern
cardinal, Carolina chickadee, yellow-billed cuckoo, dickcissel, killdeer
( Charadrius vociferus), lark sparrow ( Chondestes grammacus ), eastern
meadowlark, northern mockingbird (Mimus polyglottos), mourning dove
and painted bunting ( Passerina ciris). BBS data from the Osage and
Pidcoke route were pooled for each of these species to achieve better
representation of the area around Aquilla Lake. Confidence interval
tests of =0 for northern cardinal, Carolina chickadee, mourning
dove, painted bunting, yellow-billed cuckoo and dickcissel showed no
significant decline for the time frame of this study (P > 0.05, n = 27,
df = 25) . Negative trends in abundance were found for eastern meadow
larks, northern bobwhite, killdeer, lark sparrows and northern mocking¬
birds (P < 0.05, n = 27, df =25).

Discussion

The decline of terrestrial birds in the Aquilla Lake area over the
course of this study was apparent in density, species diversity and
species richness values. The greatest reduction in bird abundance

RANSOM & SLACK

193

occurred between pre- impoundment and the first post- impoundment
phase. Bird densities leveled off after Aquilla Lake reached conserva¬
tion pool level in 1985. The decline in bird density was mirrored by
declines in species richness and species diversity. Results from this
study showed post- impoundment bird communities on Aquilla Lake had
fewer bird numbers, had lower species diversity and richness, and were
more similar to one another in species composition when compared to
the pre- impoundment surveys.

Analysis of BBS route data suggest that there were changes among
bird species at Aquilla Lake that were not occurring in the surrounding
region. Northern cardinals and Carolina chickadees were the two most
abundant residents during the pre- impoundment survey of 1980, and
both declined to 5 and 16% of their pre- impoundment abundance,
respectively, by 1984; this was somewhat surprising given that these two
species were not habitat specialists or forest interior obligates. Indeed,
the combined BBS data showed no significant trend in the abundance of
these two species in the surrounding region for the time period of our
study. Likewise, mourning doves, painted buntings, yellow-billed
cuckoos and dickcissels showed no trend on BBS routes, but all declined
on the Aquilla Lake study site.

The change in bird density coincided with the loss of habitat area on
the Aquilla Lake site. This apparent cause and effect relationship has
been documented by numerous studies of habitat fragmentation effects
on bird communities (Forman et al. 1976; Galli et al. 1976; Whitcomb
et al. 1977; Robbins 1980; Terbourgh 1989). Loss of habitat area
alone, however, has not always explained downward trends in songbird
populations (Ambuel & Temple 1983). Sauer & Droege (1992) reported
that over the long term, more species of neotropical migrants were
increasing than were decreasing with no association between short term
declines and changes in forest acreage. James et al. (1992) also reported
results that were not consistent with the view that neotropical migrant
warblers occupying forest habitats were declining. Hill & Hagen (1991)
analyzed population trends of North American birds and found that
many species were declining, but that declines in the past 20 years might
be in part a result of normal short-term population fluctuations.

Plant succession could also account for some of the change in
abundance among species at Aquilla Lake, especially in the old-field and
scrub/shrub habitat types. There was no active habitat management

194

THE TEXAS JOURNAL OF SCIENCE— VOL. 56, NO. 3, 2004

(e.g., prescribed fire) on the USACOE property surrounding Aquilla
Lake. Over the course of this study, old-field and scrub/shrub habitats
likely changed in floristics and structure with subsequent effects on the
avian community. This might explain some of the declines seen in
eastern meadowlarks, northern bobwhites and lark sparrows.

The ability to detect reservoir impacts was hampered by several
factors. First, land use impacts on a control area off the reservoir site
precluded direct evaluation of reservoir effects. A true control site
would have been difficult to obtain for the length of the study period,
since most of the surrounding property was privately owned and sub¬
jected to various agricultural land use practices; such practices did affect
the initial control site early in this study. Second, direct cause and
effect could not be made due to methodological differences between
transect counts and BBS counts. The reason for using BBS data was to
provide some context to the data, because published data from other
reservoir construction projects does not exist. To that end, the use of
BBS data provided tangential support of the results of this study
regarding the impacts on bird communities from reservoir construction:
some bird species declined on the reservoir site during the study period,
but showed no such trend in the surrounding area.

Given that reservoir development will continue in order to provide for
a growing Texas population, further research on existing and future
reservoir sites would seem warranted. Existing reservoirs could provide
opportunities to investigate long term effects of habitat loss and fragmen¬
tation on abundance, richness, diversity and the degree of species
recovery over time; such data would be especially valuable where they
exist in proximity to established BBS routes. New reservoir construction
projects could offer opportunities to further quantify the immediate post
construction impacts on richness, diversity and abundance of avian
communities.

Acknowledgments

We acknowledge the help of T. Harris-Haller, M. Hoy and J. Hinson
with data collection during the pre- impoundment, and the first and
second post- impoundment studies, respectively. M. Brown developed
the Aquilla Lake GIS data. This work was funded by USACOE, Fort
Worth District. Additional support was provided by the Department of
Wildlife and Fisheries Sciences at Texas A&M University.

RANSOM & SLACK

195

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Carothers, S. W. & R. R. Johnson. 1975. Water management practices and their effects
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Coppedge, B. R., D. M. Engle, R. E. Masters & M. S. Gregory. 2001. Avian response
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Croonquist, M. J. & R. P. Brooks. 1993. Effects of habitat disturbance on bird
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Douglas, D. C., J. T. Ratti, R. A. Black & J. R. Alldredge. 1992. Avian habitat
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TEXAS J. SCI. 56(3): 197-206

AUGUST, 2004

SEASONAL AND ECOLOGICAL ASSOCIATIONS OF THE
AVIFAUNA FROM SIERRA SAN ANTONIO-PENA NEVADA,
ZARAGOZA, NUEVO LEON, MEXICO.

Irene Ruvalcaba-Ortega, Jose I. Gonzalez-Rojas,

Armando J. Contreras-Balderas and Alina Olalla-Kerstupp

Laboratorio de Ornitologia, Facultad de Ciencias Bioldgicas
Universidad Autonoma de Nuevo Leon
Apart ado Postal 25-F, Cd. Universitaria
San Nicolas de los Garza, Nuevo Leon, Mexico

Abstract. — This study examined the avifauna of three vegetational communities of the
Sierra San Antonio-Pena Nevada of northeastern Mexico, from June 2001 to May 2002. A
total of 1,084 individuals were recorded, comprising 83 species, 62 genera, 31 families and
9 orders. The ecological associations of the species were as follows: Pine 40; Pine-Oak 48;
and Oak 58. The seasonal distribution of the species was: Spring 48; Summer 42; Fall 47;
and Winter 40. Based on the Shannon’s Diversity Index, the highest values were obtained
for Oak Forest (H’=3.16) and for Spring (H’=3.26).

Resumen.— El presente estudio se realizo sobre la avifauna de tres comunidades vegetales
de la Sierra San Antonio-Pena Nevada, de junio de 2001 a mayo de 2002. Se registraron
1, 084 individuos, correspondientes a 83 especies, 62 generos, 31 familias y 9 ordenes. La
distribucion ecologica de las especies fue la siguiente: Bosque de Pino, 40; Bosque Mixto,
48; y Bosque de Encino, 58. En cuanto a la distribucion estacional, se obtuvo: Primavera,
48 especies; Verano, 42; Otono, 47; e Inviemo, 40. Utilizando el Indice de Diversidad de
Shannon se obtuvieron los valores mas altos para el Bosque de Encino (HP =3. 16) y para
Primavera (HP =3.26).

Many avian studies in coniferous forests of North America have
concluded that vegetation coverage or foliage is a factor that positively
influences bird species presence, richness and abundance (Tatschl 1967;
Baida 1969; Dickson & Segelquist 1979; Beedy 1981; Anderson et al.
1983; Bazakas 1996; Guzman- Velasco 1998; Garcia et al. 1998; Daniel
& Flete 1999; Mills et al. 2000; Doherty & Grubb 2000; Latta et al.
2003). Also, in the South American Andes, the distribution of some
species is apparently determined by the vegetation type (Terborgh 1971).

Avian communities are not static but change seasonally; in fact, bird
assemblages in temperate regions are composed by permanent residents
and winter and summer visitors that vary throughout the year (e.g.,
Hilden 1965; Anderson 1972). Several studies in North American
forests have found differences in species richness, density and composi¬
tion in different seasons and habitat types (Anderson et al. 1983; Avery
& van Riper III 1989; Corcuera & Butterfield 1999; Latta et al. 2003).

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In Mexico, several researchers have established the ecological
distribution of the avian communities of some elevated orographic
formations, especially with respect to the effects of altitudinal gradients
on bird species (Miller 1955; Morales-Perez & Navarro-Siguenza 1991;
Navarro 1992; Winker 1992; Garcia et al. 1998). Previous studies on
birds diversity in Nuevo Leon are mainly inventories and generally the
locality is not mentioned (Friedmann et al. 1950; Miller et al. 1957;
Martin-del Campo 1959; Contreras-Balderas et al. 1995; Contreras-
Balderas 1997; Howell & Webb 1995). Ecological aspects of the
avifauna in the state are almost non-existent, however, Guzman-
Velasco’s (1998) study on Cerro El Potosi and Gonzalez-Iglesias’ (2001)
research on Sierra Picachos are an exception. This present effort is the
first systematic study of the avian community of Sierra San Antonio-
Pena Nevada in terms of species richness, abundance, and ecological
and seasonal distribution.

Study Site

The study area (23°52’12" to 23°40’12" N and 99°57,00M to
99° 39’ 36" W) is located in the southeastern region of General Zaragoza
municipality of Nuevo Leon. Its total area is approximately 209.57 km2
and its elevation ranges from 2,200 - 3,400 m (INEGI 1986; Arriaga et
al. 2000).

This mountainous area is also the second highest elevation of Nuevo
Leon, exhibiting diverse vegetational communities that vary from chap¬
arral ( Quercus , Dasilyrion , Agave) to fir forests {Abies- Pseudotsuga) ,
including those specific to this study: Pine Forest ( Pinus ), Pine-Oak
Forest {Pinus- Quercus) and Oak Forest {Quercus). It is situated in the
Sierra Madre Oriental, but especially in the transition zone between the
Neotropical and Neartic biogeographic regions, making this a natural
ecotone. The Sierra Pena Nevada is also considered as a Prioritary
Terrestrial Region for Conservation (Arriaga et al. 2000) and an Area
of Importance for Birds Conservation in Mexico (Arizmendi & Marquez
2000).

Materials and Methods

The study site was visited monthly from April 1996 to May 2001.
Each vegetation type was sampled once each season, using 18 point
counts and 18 mist nets (distributed in 9 stations). Point counts followed

RUVALCABA-ORTEGA ET AL.

199

Table 1. List of species and their residency status: PR = Permanent resident; SR = Summer
Resident; WR = Winter Resident; T=Transient; V = Vagrant; and * = Undetermined.

Species

Common Name
(Spanish)

Common Name Residency

(English)

Coragyps atratus

Zopilote comun

Black Vulture

Cathartes aura

Zopilote aura

Turkey Vulture

Buteo brachyurus

Aguililla cola corta

Short-tailed Hawk

Buteo albonotatus

Aguililla aura

Zone-tailed Hawk

Buteo jamaicensis

Aguililla cola roja

Red-tailed Hawk

Patagioenas fasciata

Paloma de collar

Band-tailed Pigeon

Zenaida macroura

Paloma huilota

Mourning Dove

Otus flammeolus

Tecolote ojo oscuro

Flammulated Owl

Megascops asio

Tecolote oriental

Eastern Screech-Owl

Megascops trichopsis

Tecolote ritmico

Whiskered Screech-Owl

Glaucidium gnoma

Tecolote serrano

Northern Pygmy-Owl

Micrathene whitneyi

Tecolote enano

Elf Owl

Caprimulgus vociferus

Tapacamino

cuerporrin-norteno

Whip-poor-will

Hylocharis leucotis

Zafiro oreja blanca

White-eared Hummingbird

Lampormis clemenciae

Colibri garganta azul

Blue-throated Hummingbird

Eugenes julgens

Colibrf magmfico

Magnificent Hummingbird

Selasphorus platycercus

Zumbador cola ancha

Broad-tailed Hummingbird

Trogon mexicanus

Trogon mexicano

Mountain Trogon

Melanerpes formicivorus

Carpintero bellotero

Acorn Woodpecker

Picoides villosus

Carpintero velloso-mayor

Hairy Woodpecker

Colaptes auratus

Carpintero de pechera

Northern Flicker

Lepidocolaptes sp.

Trepatroncos

Woodcreeper

Contopus sp.

Pibi

Wood-Pewee

Empidonax flaviventris

Mosquero vientre
amarillo

Yellow-bellied Flycatcher

Empidonax hammondii

Mosquero de Hammond

Hammond’s Flycatcher

Empidonax wrightii

Mosquero gris

Gray Flycatcher

Empidonax occidentalis

Mosquero barranqueno

Cordilleran Flycatcher

Empidonax sp.

Mosquero

Flycatcher

Tyrannus vociferans

Tirano griton

Cassin’s Kingbird

Vireo solitarius

Vireo anteojillo

Blue-headed Vireo

Vireo huttoni

Vireo reyezuelo

Hutton’s Vireo

Aphelocoma ultramarina

Chara pecho gris

Mexican Jay

Corvus corax

Cuervo comun

Common Raven

Stelgidopteryx serripennis

Golondrina ala serrada

Northern Rough-winged
Swallow

Poecile sclateri

Carbonero mexicano

Mexican Chickadee

Baelophus wollweberi

Carbonero embridado

Bridled Titmouse

Psaltriparus minimus

Sastrecillo

Bushtit

THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 3, 2004

200

Table 1. Cont.

Species

Common Name
(Spanish)

Common Name Residency

(English)

Sitta carolinensis

Sita pecho bianco

White-breasted Nuthatch

Sitta pygmaea

Sita enana

Pygmy Nuthatch

Certhia americana

Trepador americano

Brown Creeper

Thryomanes bewickii

Chivirfn cola oscura

Bewick’s Wren

Troglodytes aedon

Chivirin saltapared

House Wren

Regulus calendula

Reyezuelo de rojo

Ruby-crowned Kinglet

Polioptila caerulea

Perlita azulgris

Blue-gray Gnatcatcher

Polioptila melanura

Perlita del desierto

Black-tailed Gnatcatcher

Sialia sialis

Azulejo garganta canela

Eastern Bluebird

Myadestes occidentalis

Clarfn jilguero

Brown-backed Solitaire

Catharus guttatus

Zorzal cola rufa

Hermit Thrush

Turdus migratorius

Mirlo Primavera

American Robin

Toxostoma curvirostre

Cuitlacoche pico curvo

Curve-billed Thrasher

Melanotis caerulescens

Mulato azul

Blue Mockingbird

Bombycilla cedrorum

Ampelis chinito

Cedar Waxwing

Ptilogonys cinereus

Capulinero gris

Gray Silky-flycatcher

Phainopepla nitens

Capulinero negro

Phainopepla

Peucedramus taeniatus

Ocotero enmascarado

Olive Warbler

Vermivora celata

Chipe corona naranja

Orange-crowned Warbler

Vermivora crissalis

Chipe crisal

Colima Warbler

Parula superciliosa

Parula ceja blanca

Crescent-chested Warbler

Dendroica coronata

Chipe Coronado

Yellow-rumped Warbler

Dendroica towns endi

Chipe negroamarillo

Towsend’s Warbler

Dendroica occidentalis

Chipe cabeza amarilla

Hermit Warbler

Dendroica sp.

Chipe

Warbler

Mniotilta varia

Chipe trepador

Black-and-white Warbler

Wilsonia pusilla

Chipe corona negra

Wilson’s Warbler

Myioborus pictus

Chipe ala blanca

Painted Redstart

Piranga flava

Tangara encinera

Hepatic Tanager

Piranga sp.

Tangara

Tanager

Pipilo maculatus

Toqui pinto

Spotted Towhee

Pipilo fuscus

Toqui pardo

Canyon Towhee

Aimophila cassinii

Zacatonero de Cassin

Cassin ’s Sparrow

Spizella passerina

Gorrion ceja blanca

Chipping Sparrow

Spizella pallida

Gordon palido

Clay-colored Sparrow

Melospiza lincolnii

Gorrion de Lincoln

Lincoln’s Sparrow

Melospiza sp.

Gorrion

Sparrow

Junco phaenotus

Junco ojo de lumbre

Yellow-eyed Junco

Pheucticus

melanocephalus

Picogordo tigrillo

Black-headed Grosbeak

RUVALCABA-ORTEGA ET AL.

201

Table 1. Cont.

Species

Common Name
(Spanish)

Common Name
(English)

Residency

Passerina caerulea

Picogordo azul

Blue Grosbeak

Passerina cyanea

Colorfn azul

Indigo Bunting

Icterus xvagleri

Bolsero de Wagler

Black-vented Oriole

Icterus graduacauda

Bolsero cabeza negra

Audubon’s Oriole

Icterus parisorum

Bolsero tunero

Scott’s Oriole

Euphonia elegantisima

Eufonia capucha azul

Elegant Euphonia

Carduelis psaltria

Jilguero dominico

Lesser Goldfinch

Ralph (1996) with a fixed radius of 20 m for 10 minutes. Birds
captured with mist nets were banded and released. Species were
recorded following the systematic nomenclature of the A. O. U. (1998;
2000; Banks et al. 2002; Banks et al. 2003). Their permanency status
was determined on the basis of field observations and information
provided by Howell & Webb (1995). Guilds were considered following
Ehrlich et al. (1988). Shannon’s Diversity Index (1948) and Sorenson’s
Index of Similarity (1948) were used to obtain diversity and similarity
indices.

Results and Discussion

Based on records obtained by systematic sampling (point counts or
mist nets), 1,080 individuals corresponding to 83 species, 62 genera, 31
families and 9 orders were recorded (Table 1). Seventy percent (54
species) of the species were defined as permanent residents, followed in
number by winter residents with 22% (17 species), summer residents
with 4% (3 species), transients with 3% (2 species), and vagrants with
1% (1 species).

The Oak Forest contained the highest number of species and individu¬
als (58 and 473, respectively), followed by Pine-Oak Forest (48 and
360, respectively), and finally Pine Forest (40 and 251, respectively).
The avian community appears distributed into discrete guilds (Table 2)
with insectivorous species (42 species, 73%) being the major group in
Oak Forest. It is suggested that this is determined by the availability of
food (primarly insects) in the Oak Forests, resulting from generally
more humid conditions than that of other forest types and the capacity
of Quercus bark to support a major richness and abundance of inverte¬
brates.

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Table 2. Number of avian species for guilds and type of vegetation.

Guilds

Total

Pine

Forest

Pine-Oak

Forest

Oak

Forest

# Sp.

tt Sp.

# Sp.

Carrion

2.4

2.5

2.1

3.4

Prey

4.8

7.5

4.2

1.7

Insectivorous

72.8

Granivorous

4.8

6.2

6.8

Nectivorous

4.8

8.3

5.1

Omnivorous

3.4

2.5

4.2

3.4

Frugivorous

4.8

2.5

6.8

Table 3. Similarity Matrix for vegetational communities (Sorenson’s Index).

Pine

Pine-Oak

Oak

Forest

Pine Forest

0.465

0.403

Pine-Oak Forest

0.485

Although Shannon diversity values were very similar across vegeta¬
tion types, the highest was the Oak Forest (FF = 3.16), followed by
Pine Forest (FT = 2.84), and lowest for Pine-Oak Forest (FT = 2.75).
Evenness values were similar across all vegetation types; ranging in
value from 0.71 (Pine-Oak Forest) to 0.78 (Oak Forest) to 0.77 (Pine
Forest). The Pine-Oak Forest showed the lowest evenness values as a
consequence of lower homogeneity in the avian community compared to
the other vegetational associations.

The least similar avian communities based on Sorenson’s Index were
Oak Forest and Pine Forest (Table 3), which shared only 40% of the
same species. By contrast, each of these was more similar to Pine-Oak
Forest, sharing 48.5% and 46.5% of the species, respectively.

The seasonal distribution of species diversity is shown in Figure 1 .
The high value for Spring appears to be due to the presence of late
winter and early summer migratory species in addition to permanent
residents. In Fall, there are occurrences of late summer and early

RUVALCABA-ORTEGA ET AL.

203

372

m#Sp. □# Ind.

Figure 1 . Seasonal distribution of avian richness and abundance. Numbers indicate the
number of species and individuals captured during the study period.

§H' DE

Figure 2. Shannon’s Index (H’) and evenness (E) values for each season.

Table 4. Similarity Matrix for seasons (Sorenson’s Index).

Spring

Summer

Fall

Winter

Spring

0.489

0.510

0.464

Summer

0.331

0.281

Fall

0.472

winter migrants that result in a greater number of species during this
season. Both Spring and Fall appear to be transitional seasons where the
replacement of bird species takes place. It is suspected that the high
abundance of birds during Winter is due to winter residents and transi¬
ents that migrate in numerically large groups, providing a lower homo¬
geneity in the avian community during this season (Figure 2). The
highest similarities among seasons were Spring and Fall (51 %) and the
lowest when comparing Summer and Winter (28. 1 %) (Table 4).

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THE TEXAS JOURNAL OF SCIENCE- VOL. 56, NO. 3, 2004

Conclusions

The most diverse avian communities were observed in Oak Forests
and during the Spring. However, although noticeable differences in
richness and abundance of birds exist among the vegetational communi¬
ties and seasons compared, values for diversity and evenness are very
similar. This leads the authors to conclude that avian communities in
Pine, Pine-Oak, and Oak Forests in the Sierra San Antonio-Pena Nevada
system are stable and homogenous throughout the year.

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AJCB at: arcontre@fcb.uanl.mx

TEXAS J. SCI. 56(3):207-214

AUGUST 2004

MATE GUARDING IN NORTHERN MOCKINGBIRDS
c M1MUS POLYGLOTTOS)

Rebecca Y. Bodily and Diane L. H. Neudorf

Department of Biological Sciences, Sam Houston State University
Huntsville, Texas 77341

Abstract. — The northern mockingbird, Mimus polyglottos, is a socially monogamous
passerine. Behavioral observations during the fertile (nest building and egg laying) and the
non-fertile (incubation) stages were used to determine the presence of paternity assurance
behaviors. Mockingbird pairs remained close (within 5 m) 76.3% of the time during the
fertile period. Median intrapair distance changed significantly from 4.8 m during the fertile
period to 11.3 m during the non-fertile period. Males followed females significantly more
during the fertile stage than the non-fertile stage. In addition, males sang the most during
the fertile period. The male perched higher than the female in all of the breeding stages.
Male northern mockingbird behavior was consistent with the mate guarding hypothesis.
However, an alternative hypothesis, i.e., that males remain close to females to ensure
copulation at the fertile stage, could not be rejected.

Ninety percent of bird species are considered monogamous (Lack
1968), however many of these species engage in copulations outside the
pair bond (termed extra-pair copulations or EPCs). Extra-pair fertiliza¬
tions (EPFs) result when EPCs are successful. Studies employing
modern molecular techniques show that EPFs are common in many bird
species with some populations containing 70% extra-pair young (Griffith
et al. 2002). In some species females pursue EPCs, which suggests that
they benefit from EPC behavior (Kempenares et al. 1992; Neudorf et al.
1997; Double & Cockburn 2000). Potential benefits of EPFs to females
include better quality genes for the offspring (Fujioka & Yamagishi
1981; Kempenaers et al. 1992; Burley et al. 1994; Hasselquist et al.
1996), increased genetic variability of the offspring (Birkhead 1993;
Petrie et al. 1998) or material benefits such as being allowed to feed on
the territory of extra-pair males (Gray 1997). In addition, the extra-pair
males may direct aggression toward predators on the territories of their
extra-pair females (Gray 1997).

In many bird species, mate guarding is a common paternity assurance
behavior (reviewed in Birkhead & Moller 1992). Mate guarding is
defined as any behavior that functions to reduce the likelihood of
encounters between a female and other males during the time when the
female is fertile (Hatch 1987). A common form of mate guarding is
closely following a mate during her fertile period (Beecher & Beecher
1979; Birkhead et al. 1987; Ritchison et al. 1994). Such behavior may
influence a females’ behavior, for example, in pied flycatchers ( Ficedula

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hypoleucia) , the risk of EPCs increases as the distance between pair
members increases (Alatalo et al. 1987). Evidence suggests that an
intrapair distance greater than 10 m significantly increases the number
of EPCs and EPC attempts (Alatalo et al. 1987).

Northern mockingbirds (Mimus polyglottos) are socially monogamous
but bigamy does occur occasionally (e.g. Laskey 1941). Low EPF
frequencies (6.9% of broods, 3.1% of offspring) have been reported for
a Texas population of mockingbirds (DeLoach 1997). The low level of
EPFs may indicate mockingbirds do not regularly pursue EPCs and thus
male paternity guards would not be necessary (Birkhead & Moller
1992). Alternatively, male mate guarding may be effective in prevent¬
ing females from obtaining extra-pair matings (e.g. Chuang- Dobbs et al.
2001, but see Stutchbury and Neudorf 1998). The purpose of this study
was to determine if male northern mockingbirds use mate guarding as
a paternity assurance strategy. If mate guarding exists, it was predicted
that males would maintain a closer proximity to females, a higher
perching position than females, and would follow females more during
the fertile period than in the non- fertile period.

Methods

Species and study area— This study was conducted on the campus of
Sam Houston State University (SHSU) in Huntsville, Walker County,
Texas, during April- August 2000 and 2001 . SHSU is a 85-ha residential
campus with an abundance of trees and manicured lawn. Hedge rows,
shrubs and trees were common nesting sites of northern mockingbirds
on campus.

Mockingbirds were trapped using walk-in Potter traps baited with
mealworms. Each individual was banded with a U.S. Fish and Wildlife
aluminum band and a unique combination of three plastic color bands
for visual identification. Sex of individual mockingbirds was determined
using behavioral cues (e.g., song) and the presence of a brood patch or
cloacal protuberance.

Nests were located by following females and males and by checking
likely nest sites such as dense shrubs and low dense trees (Joern &
Jackson 1983; Means & Goertz 1983). For this study, the female’s
fertile period was defined as the period from the initiation of nest
building to the laying of the penultimate egg (Birkhead & Moller 1992),
which was typically 7-10 days.

Behavioral observations.— Over two breeding seasons, 12 different
breeding pairs were observed during either the fertile (n = 6 pairs, 1 1

BODILY & NEUDORF

209

h) or nonfertile (n = 6 pairs, 9 h) stages. Ideally, the same female
would have been watched during both the fertile and nonfertile stage,
however, predation and nest desertion were common on the study site
making observations throughout the nesting cycle difficult. No pairs
were feeding fledglings from a previous brood at the time of observa¬
tions but some of the nests were the second or third nesting attempt for
the season. To determine if and to what extent mate guarding took
place, the behavior of individual pairs was sampled during two, 1-h
observation periods during the females’ fertile (nest building and egg
laying) or nonfertile (incubation) period. Watches were conducted only
on pairs whose nest had been located and thus their nest stage was
known at the time of the watches. Incubation watches included time
females spent on and off the nest. Nest predation and inclement weather
prevented two observations from being completed on 4 pairs. Thus, 1
pair at the fertile stage and 3 pairs at the nonfertile stage were watched
for 1 h only. Mate guarding behaviors quantified included: (1)
Intra-pair distance - distance (m) between a paired male and female
every 2 min; (2) Height above mate - recorded which sex was perched
higher (m) every 2 min; (3) Movement initiation - determined the
frequency that 1 pair member followed the other within 15 sec of a pair
member initiating a movement. A movement was defined as flying or
walking in a directed manner for at least 1 m from the original position;
(4) Song - recorded at 2 min intervals if the male was singing; (5)
Fights - noted any observations of fights or intrusions into the focal
territory by neighboring individuals or intrusions onto a neighboring
territory by focal individuals. Fights were defined as aggression
between two individuals that involved contact. Perch height and intra¬
pair distances were estimated visually by the observer. All observations
were conducted by RYB.

Statistical Analyses— Nonparametric statistics were used due to
non- normal data and small sample sizes. Behavior at fertile and
non- fertile stages was compared with Mann- Whitney U tests. Wilcoxon
signed-rank tests were used to compare male and female behavior. All
tests are one-tailed unless indicated otherwise. StatView, V. 5 (SAS
Institute, Inc., Cary, NC) was used for all analyses.

Results

Males remained closer to their mates during the fertile period than
during the non- fertile period (Table 1). Males were also within 5 m of
the female significantly more during the female’s fertile period (Mann
Whitney U test, U = 0.0, P = 0.002), with males within 5 m of

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Table 1 . Median (lower, upper interquartile range values) of mate guarding behaviors of
northern mockingbirds during the fertile and nonfertile stages.

Variable a

Fertile
n = 6

Nonfertile
n = 6

Intra-pair distance (m)

4.8

(3.7, 5.3)

11.3

(9.7, 15.5)

0.0

0.002

Time male is < 5 m

23.3

(20.0, 26.0)

10.5

(2.0, 12.0)

0.0

0.002

Male follows female

2.8

(1.0, 3.0)

0.5

(0, 2.0)

7.0

0.038

Female follows male

1.5

(1.0, 2.0)

0.3

(0, 1.0)

7.0

0.072 c

Male perched above female

14.8

(13.5, 15.5)

15.5

(13.5, 21.0)

14.5

0.285

Female perched above male

3.8

(3.0, 4.0)

5.5

(3.5, 9.0)

11.0

0.26 c

Neither perched higher

12.3

(10.5, 13.0)

8.5

(5.0, 12.5)

10.5

0.228

Male song

17.5

(14.5, 18.0)

10.0

(4.0-13.0)

6.5

0.032

Male fighting

0.0

(0, 1.0)

.75

(0, 1.0)

14.5

0.271

a Time within 5m, perching and male song are measured as number of 2-min intervals the
individuals engaged in behavior. Following and fighting are reported as actual number
of times the behaviors occurred.

b Fertile and non-fertile stages were compared with a Mann- Whitney test: U values and
P values are adjusted for ties.

c Indicates two-tailed tests.

females 76.3% of the time during the fertile period and 25.8% of the
time during the non-fertile period.

Males also followed mates more during the fertile period than the
non-fertile periods (U = 7.0, P — 0.038, Table 1). Females exhibited
a similar tendency, but differences were not significant. During the
fertile period, females initiated 64.2% of the pair movements and males
initiated 35.8%, and this difference approached significance (Wilcoxon
signed-rank test, z = -1.9, P = 0.058, two-tailed).

During the fertile period, males more often perched higher than
females perched higher (z = -2.2, P = 0.014). However, the number
of 2-min intervals during which males were perched higher than females
was not significantly different between the fertile and non-fertile periods
(U = 14.5, P = 0.29, Table 1). In 40.9% of the time intervals during
the fertile stage and 27.1% of the non-fertile time intervals, neither pair
member was perched higher than the other and this behavior did not

BODILY & NEUDORF

211

differ between nest stages (Table 1).

The average percent time males spent singing was 57% during the
fertile period, which declined to 33% during incubation. There was a
significant difference in song frequency between the fertile and non-
fertile stages (U = 6.5, P = 0.032). There was no difference in male
fighting behaviors between breeding stages (Table 1). No copulations
or copula- tion attempts were observed during observation periods.

Discussion

These findings support the mate guarding hypothesis. Male northern
mockingbirds spent more time within 5 m of mates when they were
fertile than when they were non- fertile. This behavior may function to
prevent other males from approaching and pursuing EPCs with their
mates (Birkhead & Moller 1992). Males also followed females more
during the fertile period (Table 1) and this may act to maintain proximi¬
ty (e.g., Beecher & Beecher 1979; Dickinson & Leonard 1996).

Male mockingbirds perched higher than females during both the
fertile and non- fertile periods. Therefore, this behavior is probably not
specific to mate guarding. A higher perching position may permit males
to more easily defend their territories, observe neighboring females for
extra-pair mating opportunities and be vigilant for predators (Carlson et
al. 1985). Hobson and Sealy (1989) found that male yellow warblers
( Dedroica petechia) perched higher than females throughout the nesting
cycle and they also suggested multiple benefits to this behavior in
addition to a possible mate guarding function.

Song output by male mockingbirds was more frequent during the
fertile period, which agrees with previous mockingbird studies (Logan
1983). Moller (1991) reported that males may use song in a mate
guarding context, however this does not appear to be the case in
mockingbirds. Logan (1988) found playbacks of song during the fertile
period did not elicit more aggressive responses in male mockingbirds
than did playbacks at incubation. If song functioned in mate guarding
then males would be expected to respond to playbacks more aggressively
while their mates were fertile.

Studies of the effectiveness of mate guarding have generated equivocal
results (e.g. Alatalo et al. 1987; Moller 1987; Kempenaers et al. 1995).
Despite intense mate guarding relatively high EPFs still occur in many
passerine species (e.g. Kempenaers et al. 1995; Wagner et al. 1996).
The fact that mockingbirds have such low EPFs may indicate they do
not regularly pursue EPFs or that males are extremely effective in

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preventing EPFs. The frequency of EPFs in one population of northern
mockingbirds is relatively low (6.9% of 130 broods contained extra-pair
young, Deloach 1997) compared to many other passerines (see Griffith
et al. 2002). Although EPFs can vary between populations of the same
species (Bjornstad & Litjeld 1997), there is no reason to expect this
population would have a significantly different EPF frequency than that
reported by Deloach (1997). The population is located in a similar
habitat (urban college campus) and is located only 120 km north of
Deloach’s population.

Alternative hypotheses may explain male proximity to the female at
the fertile stage (Birkhead & Moller 1992; Dickinson & Leonard 1996).
The “copulation access hypothesis” states that males remain close to
females more often at the fertile stage to increase within-pair copulation
opportunities. This hypothesis predicts males should remain close to
females during the times when copulations are more likely to occur
(Birkhead and Moller 1992). In many species, copulations occur most
frequently in the morning (e.g. Birkehead et al. 1987) whereas in others
there is no diurnal pattern (e.g. Vernier et al. 1993; Hanski 1994). To
the author’s knowledge, the timing of within-pair copulations in mock¬
ingbirds has not been studied. To test the copulation access hypothesis,
observation trials would be needed at different times throughout the day.
Presumably males should remain closer to their mates in the morning (or
the time of day that copulations normally occur) if it increases their
opportunities for copulation. Conversely, males maintaining proximity
for mate guarding purposes should be vigilant throughout the day as
extra-pair copulations can potentially occur at any time of day (Venier
et al. 1993).

The “predation hypothesis” states that males maintain proximity to
females to act as sentinels and warn females when predators are near.
This hypothesis predicts that both males and females should equally
attempt to remain in close proximity to facilitate male vigilance
(Dickinson & Leonard 1996). However, it was found that male mock¬
ingbirds were more likely to follow females than the reverse, which
supports the mate guarding hypothesis.

In conclusion, male northern mockingbirds exhibited behaviors
consistent with paternity assurance strategies. Males remained closer
and followed their mates more frequently at the fertile stage. These
behaviors have typically been regarded as methods to prevent females
from engaging in EPCs. However, one cannot completely rule out
alternative explanations for the observed behaviors. Future studies
should focus on potential extra-pair mating tactics in mockingbirds to

BODILY & NEUDORF

213

determine the extent to which mate guarding behavior may be selected
for in males.

Acknowledgments

We are grateful to C. Logan, E. Morton and B. Stutchbury for hints
on capturing mockingbirds. A. Dewees, G. Ritchison, M. Thies and
anonymous reviewers provided valuable comments on the manuscript.
Financial and logistical support was provided by Sam Houston State
University.

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DLHN at: bio_dln@shsu.edu

TEXAS J. SCI. 56(3):215-222

AUGUST, 2004

A LATE CRETACEOUS DUROPHAGUS SHARK,
PTYCHODUS MARTINI WILLISTON, FROM TEXAS

Shawn A. Hamm1 and Kenshu Shimada2

department of Geology, Wichita State University
1845 Fairmount Street, Wichita, Kansas 67260
Environmental Science Program and Department of Biological Sciences
DePaul University, 2325 North Clifton Avenue
Chicago, Illinois 60614 and

Sternberg Museum of Natural History, Fort Hays State University
3000 Sternberg Drive, Hays, Kansas 67601

Abstract.— The Late Cretaceous durophagus shark previously described as Ptychodus
connellyi (Family Ptychodontidae) by MacLeod & Slaughter is here diagnosed as a junior
synonym of Ptychodus martini Williston. The occurrence of the holotype (SMU-SMP 6903 1 )
in the Roxton Limestone Member (upper Lower Campanian) of the Gober Chalk in Fannin
County, Texas is significant both geographically and stratigraphically. Whereas the present
fossil record suggests that P. martini is endemic to the Western Interior Sea, this specimen
represents the only record of P. martini outside Kansas. If the tooth was not subjected to
any significant reworking, the specimen not only represents the youngest occurrence for the
species, but also one of the youngest occurrences of the genus and family.

Ptychodus is a Cretaceous shark genus occurring in Albian to Early
Campanian marine deposits of North and South America, Europe, Africa
and Asia (Cappetta 1987). The genus is known primarily by its teeth,
which are characterized by a massive crown suited for crushing shelled
macroinvertebrates (durophagy: e.g., see Kauffman 1978; Stewart
1988a). Based on articulated specimens (e.g., MacLeod 1982), teeth
were arranged in parallel rows in both the upper and lower jaws,
forming a pavement-like dentition.

Species of Ptychodus are differentiated on the basis of variations in
dental morphology (e.g., Cappetta 1987). The tooth crown of
Ptychodus is generally square to rectangular when viewed occlusally,
and the central portion of the crown surface has several parallel or radial
ridges. Surrounding the central portion of the crown is the marginal
area, which exhibits various textural patterns (e.g., granular, concentric,
radial) formed by numerous small ridges, pits and tubercles. The crown
rests on top of a massive tooth root, which may be weakly bilobed. The
tooth root is smaller in dimension than the crown and has many forami¬
na located at the crown-root interface. The criteria used to distinguish
various species of Ptychodus include crown height, the configuration and
number of ridges on the tooth crown, and the ornamentation on the
marginal area.

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THE TEXAS JOURNAL OF SCIENCE— VOL. 56, NO. 3, 2004

Figure 1. Ptychodus martini Williston 1900a: (A) Occlusal view of SMP-SMU 69031 from
Roxton Limestone Member (upper Lower Campanian) of Gober Chalk, Texas, initially
described as P. connellyi MacLeod & Slaughter 1980; (B) basal view of SMP-SMU
69031; (C) anterior view of SMP-SMU 69031; (D) occlusal view of FHSM VP-2121
from Smoky Hill Chalk Member of Niobrara Chalk, Kansas; (E) basal view of FHSM
VP-2121 ; (F) occlusal view of one of the teeth in holotype of P. martini (KUVP 55277:
see Fig. 1G) from Smoky Hill Chalk Member of Niobrara Chalk, Kansas, which
resembles SMP-SMU 69031 and FHSM VP-2121; (G) entire view of holotype of P.
martini (KUVP 55277: arrow points to tooth shown in Fig. IF). Scale bar = 5 mm.

MacLeod & Slaughter (1980) described a new species of Ptychodus ,
P. connellyi , based on a single tooth (Figs, la-c) recovered from the
Roxton Limestone Member (Lower Campanian) of the Upper Cretaceous
Gober Chalk (Fig. 2) in northeastern Texas. This specimen (the holo¬
type) remains the only known example of the species (Welton & Farish
1993, p. 58). However, comparisons with other Ptychodus specimens
suggest that P. connellyi is conspecific with another species, P. martini
(Williston 1900a). Therefore, the purpose of this paper is to reinterpret
the holotype as P. martini , and discuss the geographic and stratigraphic
significance of the specimen. Specimens in the following institutions are
discussed in this paper: Fort Hays State University, Sternberg Museum
of Natural History (FHSM), Hays, Kansas; the University of Kansas
Vertebrate Paleontology Collection (KUVP), Lawrence, Kansas and the
Shuler Museum of Paleontology at Southern Methodist University
(SMP-SMU), Dallas, Texas.

HAMM & SHIMADA

217

! CHRONOLOGIC UNIT

KANSAS

TEXAS

Period

Stage

Group

Formation

Group

Formation

Late

Pierre

Lake Creek

Pecan Gap

Weskan

>»

Wolf City |

Sharon Springs

Ozan

Roxton SMP-SMU 69031

Gober

C/>

Late

CO
•*- •

‘c

Middle

Smoky Hill

«z

Austin

€0

.ate

KUVP 55271, FHSM VP-2121

’c

Early

Fort Hays

Atco

Figure 2. Generalized Upper Cretaceous stratigraphy (formations and members) of western
Kansas and northeastern Texas (after Kennedy et al. 1997), indicating the stratigraphic
horizons of Ptychodus martini specimens.

Systematic Paleontology
Ptychodus martini Williston 1900a

Material.— SMP-SMU 69031 (Figs, la-c), a single tooth initially
described as Ptychodus connellyi MacLeod & Slaughter (1980).

Occurrence.— Roxton Limestone Member of the Gober Chalk (Fig.
2) exposed along the banks of Brushy Creek, 1.5 miles (2.4 km)
southeast of the town of Barkley Woods, Fannin County, Texas
(MacLeod & Slaughter 1980: Fig. 3).

Description.— SMP-SMU 69031 is rectangular when viewed
occulusally and measures 37 mm wide and 21 mm in anteroposterior
length. The crown is flat and measures only 5 mm in height. Eight low
transverse ridges extend over much of the surface, and the marginal area

218

THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 3, 2004

Figure 3. Geographic distribution of Ptychodus martini teeth recovered.

is very narrow and smooth lacking any ornamentation. However, this
lack of ornamentation appears to be due to weathering as the tooth exhi¬
bits signs of abrasion. The tooth root is tabular and porous, and lacks
a nutrient groove. The total tooth height (crown -I- root) is 16 mm.

Discussion

Taxonomic remarks.— Based on SMP-SMU 69031, MacLeod &
Slaughter (1980) differentiated Ptychodus connellyi from all other
Ptychodus species by the flat occlusal surface (i.e., without an elevated

HAMM & SHIMADA

219

cusp). However, observations suggest that the morphology of SMP-
SMU 69031 (Fig. la-c) closely resembles teeth from the median row in
the holotype of P. martini (KUVP 55277: Figs, lf-g) and FHSM-2121
(Figs, ld-e) recovered from the Upper Cretaceous Smoky Hill Chalk
Member of the Niobrara Chalk in western Kansas. Because of their
close resemblance, and the fact that no other Ptychodus species possess
rectangular teeth with a flat occlusal surface (e.g., see Cappetta 1987;
Wei ton & Farish 1993), the authors consider P. connellyi to be con-
specific with P. martini. Because P. martini Williston (1900a) was
described earlier than P. connellyi MacLeod & Slaughter (1980), P.
connellyi is considered a junior synonym of P. martini following the
International Code of Zoological Nomenclature (ICZN 1999).

Anatomical remarks. —The holotype of Ptychodus martini (Fig. lg)
consists of a set of 1 10 teeth. Although they were discovered disassoci¬
ated, the teeth presumably come from an individual shark and were
arranged artificially (for naturally arranged, general dental pattern of
Ptychodus , see Woodward 1911). The occlusal surfaces of some teeth
in the specimen are exceptionally flat and possess low, thin transverse
ridges that extend fully to the marginal area. These are interpreted to
come from the median tooth row because they are the largest, most
symmetrical teeth in the dentition. Other teeth in the dentition, which
are interpreted to represent teeth of lateral rows, are less elongate and
have a slightly elevated crown with wider marginal areas. The mor¬
phology of SMP-SMU 69031 (Figs, la-c) suggests that the tooth is from
the medial tooth row (cf. Fig. If).

Geographic remarks.— Reports on Ptychodus martini are scarce. The
only previously reported specimens are KUVP 55277 (holotype:
Williston 1900a; 1900b; Schultze et al. 1982, p. 13; Fig. lg) and FHSM
VP-2121 (isolated tooth: Hamm 2002; Figs, ld-e) from western Kansas.
The occurrence of P. martini in Texas is significant because it extends
the geographic distribution of the species from the Western Interior to
near the Gulf of Mexico (Fig. 3). Nevertheless, the present fossil
record suggests that P. martini is endemic to the Western Interior Sea.

Stratigraphic remarks.— The genus Ptychodus had a nearly worldwide
distribution from Albian to Campanian time (Cappetta 1987; Welton &
Farish 1993). The two previously reported P. martini specimens
(KUVP 55277 and FHSM VP-2121) occurred in the Smoky Hill Chalk
Member of the Niobrara Chalk (Fig. 2). Stewart (1990, p. 24) noted

220

THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 3, 2004

that P. martini occurs only in his Proto sphyraena pemicosa biozone
(Stewart 1988b). This biozone corresponds to Hattin’s (1982) lithostrati-
graphic Marker Units 1, 2 and 3, which are collectively Late Coniacian
in age.

In northeastern Texas, the Gober Chalk is interpreted to be the upper
tongue of the Austin Chalk (Stephenson 1927). The uppermost part
(0.3-3 m) of the Gober Chalk, referred to as the Roxton Limestone (Fig.
2), consists of skeletal limestone rich in inoceramid [ Inoceramus balticus
(Boehm)] and ammonite remains (Fisher 1965). The occurrence of the
ammonites Menabites delawarensis (Morton) and Scaphites hippocrepis
(deKay) dates the Roxton Limestone as late Early Campanian in age
(Cobban & Kennedy, 1992).

The surface of the Ptychodus martini tooth described in this paper
(SMP-SMU 69031) shows extensive signs of abrasion (Figs. la-c). The
abrasion could have resulted from a combination of pre-burial deposi-
tional activities and/or reworking. Because it was recovered from the
banks of Brushy Creek (Macleod & Slaughter 1980), the abrasion may
also be due to modern fluvial processes. It should be noted that the only
Upper Cretaceous rocks in which Brushy Creek cuts through are the
Gober Chalk (including the Roxton Limestone) and the overlying Ozan
Formation (Fig. 2) where it intersects with the main channel of the
North Sulphur River (based on UTBEG 1966; Mark McKenzie pers.
comm. 2002).

Ptychodus has been reported from the Albian to the Campanian in
North America (e.g., Williston 1900a; Applegate 1970; Meyer 1974;
Cappetta 1987). Dibley (1911) reported 17 teeth of P. poly gyrus
Agassiz from northern France in the zone of Actinocamax quadratus (De
Blaiville), which is Early Campanian in age. Schwimmer & Williams
(1994) reported the occurrence of P. mortoni in an early Early Campani¬
an deposit in eastern Alabama. If indeed SMP-SMU 69031 occurred in
the Roxton Limestone (with no or insignificant reworking) , the specimen
is important because it represents the youngest occurrence of P. martini
(giving the stratigraphic range of the taxon from Late Coniacian to late
Early Campanian). Together with Dibley (1911) and Schwimmer &
William’s (1994) data, the specimen also marks one of the youngest
occurrences for the genus Ptychodus and family Ptychodontidae (see also
Cappetta et al. 1993).

HAMM & SHIMADA

221

Acknowledgments

We thank the following individuals for allowing us access to
specimens in their care: R. J. Zakrzewski (FHSM); D. Maio (KUVP)
and K. Newman (SMU). The senior author would also like to thank M.
McKenzie (Grapevine, Texas) for discussions on the geology of the
Gober Chalk, as well as his wife, Amy Hamm, for her help and
support. We would also like to thank David Cicimurri (Bob Cambell
Geology Museum, Clemson, South Carolina) and David Schwimmer
(Columbus State University, Columbus, Georgia) for their reviews and
comments.

Literature Cited

Applegate, S. P. 1970. The vertebrate fauna of the Selma Formation of Alabama. VIII,
The fishes. Fieldiana, Geol. Mem., 3(8) :383-433 .

Cappetta, H. 1987. Chondricthyes II. Mesozoic and Cenozoic Elasmobranchii. Pp. 1-193,
in Handbook of Paleoicthyology: Volume 3B (H.-P. Schultze, ed.), Gustav Fischer
Verlag, Stuttgart, 193 pp.

Cappetta, H., C. Duffin & J. Zidek. 1993. Chondrichthyes. Pp. 593-609, in The Fossil
Record 2 (M. J. Benton, ed.), Chapman & Hall, London, 845 pp.

Cobban, W. A. & W. J. Kennedy. 1992. Campanian ammonites from the Upper
Cretaceous Gober Chalk of Lamar County, Texas. J. Paleont., 66(3):440-454.

Dibley, G. E. 1911. On the teeth of Ptychodus in the English Chalk. Quart. J. Geol. Soc.
London, 67:263-277.

Fisher, W. J. 1965. Rock and mineral resources of East Texas. Univ. Texas, Bureau
Econ. Geol. Rep. Invest., 54:1-439.

Hamm, S. A. 2002. First occurrence of Ptychodus martini (Ptychodontidae) from the
Roxton Member of the Gober Chalk. J. Vert. Paleont., 22(Supp. to No. 3):62A.

Hattin, D. E. 1982. Stratigraphy and depositional environment of Smoky Hill Chalk
Member, Niobrara Chalk (Upper Cretaceous) of the type area, western Kansas. Kansas
Geol. Survey Bull., 225:1-108.

ICZN (International Commission on Zoological Nomenclature). 1999. International Code
of Zoological Nomenclature (fourth edition). International Trust for Zoological
Nomenclature, London, 308 pp.

Kauffman, E. G. 1978. Ptychodus predation upon a Cretaceous Inoceramus. Palaeont.,
15:439-444.

Kennedy, W. J., W. A. Cobban & N. H. Landman. 1997. Campanian ammonites from the
Tombigbee Sand Member of the Eutaw formation, the Mooreville Formation, and the
basal part of the Demopolis Formation in Mississippi and Alabama. American Museum
Novitates, 3201:1-44.

MacLeod, N. 1982. The first North American occurrence of the Late Cretaceous
elasmobranch Ptychodus rugosus Dixon with comments on the functional morphology of
the dentition and dermal denticles. J. Paleont., 56:403-409.

MacLeod, N. & B. Slaughter. 1980. A new ptychodontid shark from the Upper Cretaceous
of northeast Texas. Texas J. Sci., 32(4): 333-335.

Meyer, R. L. 1974. Late Cretaceous elasmobranchs from the Mississippi east Texas
embayments of the Gulf Coastal Plain. Unpublished Ph.D. dissertation, Southern

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Methodist Univ., Dallas, Texas, 419 pp.

Schultze, H.-P., J. D. Stewart, A. M. Neuner & R. W. Coldiron. 1982. Type and figured
specimens of fossil vertebrates in the collection of the University of Kansas Museum of
Natural History. Part I. Fossil fishes. Misc. Pub. Univ. Kansas Mus. Nat. Hist.,
73:1-53.

Schwimmer, D. & G. D. Williams. 1994. Vertebrate-based Upper Cretaceous
biostratigraphy for the Gulf and Atlantic Coastal Plains. J. Vert. Paleont., 14(Supp. to
No. 3):56A.

Stephenson, L. W. 1927. Notes on the stratigraphy of the Upper Cretaceous formations of
Texas and Arkansas. Bull. Am. Asso. Petrol. Geol., 11:1-17.

Stewart, J. D. 1988a. Paleoecology and the first North American West Coast record of the
shark genus Ptychodus. J. Vert. Paleont., 8(Supp. to No. 3):27A.

Stewart, J. D. 1988b. The stratigraphic distribution of Late Cretaceous Protosphyraena in
Kansas and Alabama. Fort Hays Studies (Third Ser.), 10:80-94.

Stewart, J. D. 1990. Niobrara Formation vertebrate Stratigraphy. Pp. 19-30, in Niobrara
Chalk Excursion Guidebook (S. C. Bennett, ed.), Univ. Kansas Mus. Nat. Hist. &
Kansas Geol. Survey, Lawrence, 81 pp.

UTBEG (University of Texas Bureau of Economic Geology). 1966. Geologic Atlas of
Texas, Texarkana Sheet. Univ. Texas Bureau Econ. Geol., scale 1:250,000.

Welton, B. & R. F. Farish. 1993. The collectors guide to fossil sharks and rays from the
Cretaceous of Texas. Before Times, Lewisville, Texas, 204 pp.

Williston, S. W. 1900a. Some fish teeth from the Kansas Cretaceous. Kansas Univ.
Quart., 9:27-42.

Williston, S. W. 1900b. Cretaceous fishes, selachians and ptychodonts: Univ. Geol.
Survey Kansas, 6(2):237-255.

Woodward, A. S. 1911. The fishes of the English Chalk. Palaeontogr. Soc., London,
6:185-224.

SAH at: sahamm@sbcglobal.net

TEXAS J. SCI. 56(3):223-230

AUGUST, 2004

NEW RECORDS OF THE TEXAS HORNSHELL
POPENAIAS POPEll (BIVALVIA: UNIONIDAE)

FROM TEXAS AND NORTHERN MEXICO

Ned E. Strenth, Robert G. Howells
and Alfonso Correa-Sandoval

Department of Biology, Angelo State University
San Angelo, Texas 76909,

Texas Parks and Wildlife Department, HOH Fisheries Science Center
HC07, Box 62, Ingram, Texas 78025 and
Laboratorio de Zoologi'a, Instituto Tecnologico de Cd. Victoria
A.P. 175, C.P. 87010, Cd. Victoria, Tamaulipas, Mexico

Abstract.— The Texas hornshell (Popenaias popeii) is reported and documented from the
South Concho River in west central Texas and the Rio Sabinas of northern Coahuila, both
new site records. These records confirm the known distributional range of this species in
the Colorado River drainage of central Texas and establishes a new interior state record for
Coahuila. Recently collected shell material of P. popeii is also reported from the Devils
River above Amistad Reservoir and from the Rio Salado above Falcon Reservoir.

Resumen.— El bivalvo texano conocido como concha cuerno ( Popenaias popeii ) es
registrado en el Rio Concho Sur en el centro-oeste de Texas y el Rio Sabinas en el norte de
Coahuila. Ambos sitios son nuevos registros geograficos. Estos registros confirman el
ambito de distribution conocido de la especie en el drenaje del Rio Colorado del centro de
Texas y establece un nuevo registro estatal interior para Coahuila. Especimenes de P. popeii
tambien son registrados en el Rio Devils arriba de la Presa La Amistad y en el Rio Salado
arriba de la Presa Falcon.

The freshwater bivalve Popenaias popeii was originally described
from the "Devil’s River and Rio Salado, Texas" by Lea (1857) as Unio
popeii. Both the designation of the type-locality as well as the scientific
name have undergone subsequent revision. While the designation of the
Devils River as one of the original collection sites of P. popeii by Lea
(1857) is undisputed by subsequent authors, some confusion existed
early relative to the exact location of the Rio Salado. Lea (1857)
originally placed it in "Texas". Stearns (1891) gave the location as
"near Leon, Mexico" and noted additional specimens from the "Rio
Salado, New Mexico"; Singley (1893) referred to its location as "New
Mexico" and Simpson (1914) cited its location as "New Leon, Mexico"
(state of Nuevo Leon). Johnson (1999:21) noted that the lectotype
USNM 85895 from the Rio Salado in Nuevo Leon was "inadvertently"
selected by Johnson (1974:115) as the "figured holotype."

The Texas hornshell historically ranged south in the coastal systems
of northeastern Mexico to at least the Rio Cazones of Vera Cruz

224

THE TEXAS JOURNAL OF SCIENCE— VOL. 56, NO. 3, 2004

(Johnson 1999). In addition to the Devils River and Rio Sal ado, it has
been found upstream in the Pecos River to Ward County in Texas
(Singley 1893) and several locations in New Mexico (Cockerell 1902;
Metcalf 1982; Lang 2000); upstream in the Rio Grande to sites just
downstream of Big Bend, Brewster County, Texas (Howells 1994) as
well as several Mexican tributaries of the lower Rio Grande (Johnson
1999). A shell found in the Llano River in 1972 at Castell in Llano
County (Ohio State University Museum collection OSUM 1976.365) was
reported by Howells et al. (1997). Both Howells (2001a) and Smith et
al. (2003) have recently mapped the distribution of P. popeii from the
drainage systems of Texas, New Mexico and northern Mexico.

As a result of recent field collections, this report documents additional
range extensions for Popenaias popeii from west-central Texas and
northern Coahuila. Additionally, recent examinations of several pre¬
viously known collection localities were conducted in both Texas and
Mexico. Voucher specimens are deposited with the holdings of the
Illinois National History Survey (INHS), the Instituto Tecnologico de
Ciudad Victoria (ITCV) and the Angelo State University Natural History
Collections (ASNHC). The following listing is abbreviated and cites
only those synonymies/citations deemed relevant to this study.

Popenaias popeii (Lea 1857)

Texas Hornshell

Unio popeii.— Lea 1857:102; Binney 1863:387; Cockerell 1902:69; Diaz
de Leon 1912:136; Simpson 1914:700; Johnson 1974:115.

Unio pop ei. — Stearns 1891:104; Singley 1893:322.

Elliptio popei . — Ortmann 1912:271; Strecker 1931:17; Murray & Roy
1968:26.

Elliptio ( Popenaias ) popei.— Frierson 1927:38.

Nephronaias ( Popenaias ) popeii.— Haas 1969:201.

Popenaias popei.— Heard & Guckert 1970:339; Burch 1973:16; Neck
1984:11; Neck & Metcalf 1988:262; Howells et al. 1996:93; Johnson
1999:21.

Popenaias popeii.— Metcalf 1982:45; Howells 2001 a: 62; Smith et al.
2003:333.

STRENTH, HOWELLS & CORREA

225

New Records

South Concho River. — A single left valve was collected in 1991 from
among flotsam at the low water crossing of the South Concho River and
U.S. Highway 277 within the city limits of Christoval, Texas. Heavy
flooding had occurred in the area several weeks prior to the collection
date.

Material examined. — South Concho River in Christoval (N 3 1 ° 1 1’ 15"
W 100°29’59"), Tom Green County, Texas, 21 July 1991, a single left
valve (INHS 29012).

Remarks.— All previous records of Popenaias popei from Texas
except the single specimen from the Llano River reported by Howells
et al. (1997) have been made from the Rio Grande or its tributaries.
This current record is noteworthy in that the South Concho River, like
the Llano River, is a tributary of the Colorado River drainage system.
The exact nature of the significance of these distributional records of P.
popeii from the Colorado River drainage currently remains unknown.
Numerous additional collections by Texas Parks and Wildlife Depart¬
ment from 1992 through the present failed to find any other specimens
of P. popeii in the Llano or Concho rivers, or elsewhere in the Colorado
drainage basin (Howells 2001b). Collected along with the single speci¬
men of P. popeii were several single valves of Cyrtonaias tampicoensis
(Tampico pearly mussel).

Rio Sabinas.— Specimens of Popenaias popeii were initially collected
from the dry river bed of the Rio Sabinas in the Rio Los Sabinitos Park
area on Highway 20 (Coahuila) just west of Rio Villa de San Juan
Sabinas, Coahuila in August of 2001. A second collection in January
of 2002 was made approximately 0.5 km upstream from the original
site.

Material examined.— Rio Sabinas west of Rio Villa de San Juan
Sabinas (N 27°55,23" W 101 ° 1 8’21 "), Coahuila, Mexico, 2 August
2001, three complete sets of valves (INHS 29013); 19 January 2002,
three complete sets of valves (ITCV 8002), three complete sets of valves
(ASNHC 0049).

Remarks. — Although this report represents the first interior record
(other than the Rio Grande) of nonfossil material of Popenaias popeii
from the state of Coahuila in northern Mexico, it should be noted that
the Rio Sabinas is an upstream tributary of the Rio Sal ado. At the time
of the collections in August 2001 and January 2002, the Rio Sabinas was
completely dry and without any evidence of recent water flow. Workers
in the municipality of Sabinas, approximately 20 km downstream from

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THE TEXAS JOURNAL OF SCIENCE— VOL. 56, NO. 3, 2004

the collection site, reported a cessation of water flow in the Rio Sabinas
in the spring of 2000. Dead shell material of Cyrtonaias tampicoensis
and Utterbackia imbecillis (paper pondshell) was also present in the dry
river bed.

Additionally, the Rio Sabinas was examined approximately 50 km
downstream from the municipality of Sabinas at Juarez just before the
river enters the impoundment of the Presa Don Martin (listed on some
maps as Presa Venustiano Carranza). At this location (N 27°36’42" W
100°43’29"), the river is accessible beneath the Highway 35 (Coahuila)
bridge. Metcalf (1982) earlier reported fossil material of Popenaias
popeii from this location. On 27 October 2001 and 3 March 2002 the
river exhibited no flow and was characterized by a series of large
isolated pools. Numerous intact pairs of valves of dead specimens of
Cyrtonaias tampicoensis and Utterbackia imbecillis were common along
the bank and shallow soft substrate of the stream bed. No specimens of
Popenaias popeii were found.

Previously Reported Records

In addition to collection efforts in the South Concho River and the Rio
Sabinas, both of the originally designated type-localities of the Devils
River and Rio Salado as well as the Llano River were revisited in an
effort to assess the current existence of specimens of Popenaias popeii
at each of these three different locations.

Devils River . — Considerable anthropogenic changes have occurred in
the area of the lower Devils River since the original collection of
Popenaias popeii in the 1800’s. The Amistad Reservoir Dam (Presa La
Amistad) was completed on the Rio Grande between Texas and Mexico
in 1968. The resulting lake area included the confluence of the Rio
Grande with both the Devils River and the Pecos River. Popenaias
popeii requires a shallow stream environment and is not currently known
from impoundments (Lang 2000); consequently the man-made Amistad
Reservoir does not appear to provide suitable habitat for this species.
The area of the Devils River immediately above the lake level was
examined in July of 2001.

Material examined.— 200 m upstream from the confluence of the
Devils River and Amistad Reservoir (N 29°39’54" W 100°55’58"), Val
Verde County, Texas, 14 July 2001, two complete (but damaged) sets
of valves and broken shell material from two additional specimens
(ASNHC 0050). All of the P. popeii shell material was old and
weathered; no fresh shell material was found at this location.

STRENTH, HOWELLS & CORREA

227

Remarks . — Despite changes associated with the construction of the
Amistad Reservoir Dam, that section of the Devils River immediately
above the current lake level appears to provide a physical habitat capable
of sustaining extant populations of Popenaias popeii. While the
presence of the above recently collected shell material of P. popeii in
July of 2001 would appear to support the above proposal, only addition¬
al and more detailed field studies in this area can determine the current
status of this species in the lower Devils River. Collected along with the
specimens of P. popeii in 2001 were valves of Cyrtonaias tampicoensis .

Rio Salado.— In a fashion similar to that of the Devils River, the Rio
Salado has also undergone considerable anthropogenic changes since the
original collection of Popenaias popeii in the 1800’s. Falcon Dam
(Presa Falcon) was constructed on the Rio Grande between Texas and
Mexico in 1953. The resulting Falcon Reservoir included the conflu¬
ence of the Rio Salado with the Rio Grande. As previously mentioned
in reference to Amistad Reservoir, the resulting reservoir does not
appear to provide suitable habitat for adult specimens of P. popeii. The
area of the Rio Salado above the lake level was examined in March of
2002.

Material examined. — Rio Salado 100 m downstream from bridge on
Highway 2 (Mexico) in northern Tamaulipas (N 26°47’23" W 99°25’
20"), 2 March 2002, a single heavily worn right valve (ASNHC 0051).

Remarks. — At the time of the March 2002 collection, the Rio Salado
exhibited no flowing water in the area of the Highway 2 bridge. The
river was characterized by a series of large pools, which were separated
by narrow bars of exposed substrate. Numerous intact pairs of valves
of dead specimens of Cyrtonaias tampicoensis , Utterbackia imbecillis
and Quadrula apiculata (Southern mapleleaf) were common in the
stream bed.

Anahuac.— Rio Salado beneath and downstream of the Highway 1
(Nuevo Leon) bridge within the municipality of Anahuac, Nuevo Leon
(N 27° 14’ 1.4" W 100°08’21 .9"), 2 June 2002; three complete sets of
valves and four single valves (one of the single valves was very recent)
(ASHC 0052).

Remarks.— The river at the time of the collection exhibited no detect¬
able flow and was under considerable influence of untreated household
waste pollutants. Several specimens of Cyrtonaias tampicoensis and
Utterbackia imbecillis were also found at this location.

Llano River.— A single specimen of Popenaias popeii collected in

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THE TEXAS JOURNAL OF SCIENCE— VOL. 56, NO. 3, 2004

1972 was reported by Howells et al. (1997) from the Llano River (N
30°42’ 13" W 98°57’32") and the crossing of Highway 2768 at Castell
in Llano County. Several recent visits in 1992, 1997, 1999, 2000 and
2001 to the Castell area yielded no additional specimens of P. popeii.

Corbicula sp.

Shell material of the Asian clam was present at every collection site
in both Texas and Mexico examined during the course of this study and
is therefore not individually reported as part of the additional faunal
listings.

Discussion

This study extends the known range of Popenaias popeii to include
the South Concho River of west central Texas and the Rio Sabinas of
northern Coahuila. It also confirms the earlier report of this species by
Howells et al. (1997) from the Colorado River drainage system of
central Texas.

These additional extensions to the known range of this freshwater
bivalve would initially appear to represent positive indications to the
overall conservation status of this species. It should be noted, however,
that current conditions related to reduced water flow, drying of stream
beds, or both, in the Rio Sal ado and Rio Sabinas of northern Mexico do
not appear capable of supporting significant populations of Popenaias
popeii. While isolated or protected areas of both of these rivers or their
tributaries may in fact support limited numbers of surviving individuals
or populations, the decline in suitable habitat in the area of northern
Tamaulipas, Nuevo Leon and Coahuila does not appear favorable to the
overall survivability of this species.

Even though heavy rains in April of 2004 returned the Rio Sabinas to
normal flow, the Devils, Llano and South Concho rivers of Texas cur¬
rently appear to provide a greater range of both available and seemingly
suitable habitat for maintaining Popenaias popeii than do most of the
rivers of northern Mexico. However, no extant populations are current¬
ly known from these three rivers. These rivers appear to provide both
adequate levels of water and the necessary current flow capable of main¬
taining surviving populations of P. popeii. Very little is known about
this species in Texas and no living specimens were observed during the
course of this study. The extreme rarity of recovered shell material
from both the Llano and South Concho would appear indicative of popu¬
lations at or near the extinction level in these two rivers. Indeed, the
only known populations of P. popeii are present in a short stretch of the

STRENTH, HOWELLS & CORREA

229

Black River, New Mexico (Lang 2000; Howells 2001a) and the Rio
Grande, Webb County, Texas (Howells 2003, 2004), with recently dead
shells found in the Rio Grande between Big Bend and the mouth of the
Pecos River, Texas, suggesting survivors may also persist there as well
(Howells 2004). Additional and more detailed study would be required
to determine the current status of this species in the rivers of west
central Texas. However, this study indicates that P. popeii is at least
rare or endangered throughout its range in Texas and New Mexico.

Acknowledgments

The authors wish to thank David Marsh, James Holm, Jeff Masters,
Barbara Strenth, Brad Henry, Lynn McCutchen and Kathryn Perez for
assistance in the collection of specimens during the course of this study.
Appreciation is extended to Kevin Cummings (Illinois Natural History
Survey), Arthur Bogan (North Carolina State Museum of Natural
Sciences) and two anonymous reviewers for their comments and
suggestions for improving this manuscript.

Literature Cited

Binney, W. G. 1863. Bibliography of North American Conchology Previous to the Year
1860, Smithsonian Miscellaneous Collections, Part I, 650 pp.

Burch, J. B. 1973. Freshwater Unionacean clams (Mollusca: Pelecypoda) of North
America. Biota of Freshwater Ecosystems Identification Manual 11. US Environmental
Protection Agency, 176pp.

Cockerell, T. D. A. 1902. Unio popeii, Lea, in New Mexico. The Nautilus, 16:69-70.
Diaz de Leon, J. 1912. Catalogus Molluscarum Maxicanae Reipublicae hucusque descripta.
La Naturaleza Tercera Siere, 1 (4):93- 143 .

Frierson, L. S. 1927. A classified and annotated check list of the North American Naiades.

Baylor University Press, Waco, Texas, 111 pp.

Haas, F. 1869. Superfamilia Unionacea. Das Tierreich (Berlin) 88x + 663 pp.

Heard, W. H. & R. H. Guckett. 1970. A Re-Evaluation of the Recent Unionacea
(Pelecypoda) of North America. Malacologia, 10(2):333-335.

Howells, R. G. 1994. Preliminary distributional surveys of freshwater bivalves in Texas:
progress report for 1992. Texas Parks and Wildlife Department, Management Data
Series 105, Austin, 16 pp.

Howells, R. G. 1999. Distributional surveys of freshwater bivalves in Texas: progress
report for 1998. Texas Parks and Wildlife Department, Management Data Series 161,
Austin, 28 pp.

Howells, R. G. 2001a. Status of freshwater mussels of the Rio Grande, with comments on
other bivalves. Texas Parks and Wildlife Department, Austin, 81 pp.

Howells, R.G. 2001b. Declining status of freshwater mussels of the Rio Grande, with
comments on other bivalves. Pages 59-73 in G. P. Garrett and N. L. Allan. Aquatic
fauna of the northern Chihuahuan Desert. Museum of Texas Tech University, Special
Publication 46, Lubbock, 160 pp.

Howells, R. G. 2003. Distributional surveys of freshwater bivalves in Texas: progress
report for 2002. Texas Parks and Wildlife Department, Management Data Series 214,
Austin, 35 pp.

Howells, R. G. 2004. Distributional surveys of freshwater bivalves in Texas: progress

230

THE TEXAS JOURNAL OF SCIENCE- VOL. 56, NO. 3, 2004

report for 2003. Texas Parks and Wildlife Department, Management Data Series 222,
Austin, 50 pp.

Howells, R. G., C. M. Mather & J. A. M. Bergmann. 1997. Conservation status of
selected freshwater mussels in Texas. Pages 117-129 in K.S. Cummings, A.C.
Buchanan, C.A. Mayer, and T.J. Naimo. Conservation and management of freshwater
mussels II: initiatives for the future. Proceedings of a UMRCC symposium, St. Louis,
Missouri, October 1995. Upper Mississippi River Conservation Committee, Rock Island,
Illinois, 293 pp.

Howells, R. G., R. W. Neck & H. D. Murray. 1996. Freshwater Mussels of Texas. Texas
Parks and Wildlife Department, Austin, Texas, 218 pp.

Johnson, R. I. 1974. Recent and Fossil Taxa of Unionacea and Mutelacea introduced by
Issac Lea, Including the Location of all of the Extant Types. Museum of Comparative
Zoology Special Occasional Publication, 2:1-159.

Johnson, R. I. 1999. Unionidae of the Rio Grande (Rio Bravo del Norte) System of Texas
and Mexico. Occasional Papers on Mollusks, 6(77): 1-65.

Lang, B. L. 2000. Status of the Texas homshell and native freshwater mussels (Unionoidea)
in the Rio Grande and Pecos River of New Mexico and Texas. New Mexico Department
of Game and Fish, Performance Report, Santa Fe, 17 pp.

Lea, I. 1857. Description of Six New Species of Fresh Water and land Shells of Texas and
Tamaulipas, from the Collection of the Smithsonian Institution. Proceedings of the
Academy of Natural Sciences of Philadelphia, 9(1857): 101-102.

Metcalf, A. L. 1982. Fossil Unionacean Bivalves from Three Tributaries of the Rio
Grande. Pp. 43-58, 2 plates, in Proceedings of the Symposium on Recent Benthological
Investigations in Texas and Adjacent States (J. R. Davis, Editor). Texas Academy of
Science Aquatic Sciences Section, Austin, Texas, 278 pp.

Murray, H. D. & E. C. Roy, Jr. 1968. Checklist of Freshwater and Land Mollusks of
Texas. Sterkiana, 30:25-42.

Neck, R. W. 1984. Restricted and Declining Nonmarine Molluscs of Texas. Texas Parks
and Wildlife Department Technical Series No. 34:1-17.

Neck, R. W. & A. L. Metcalf. 1988. Freshwater Bivalves of the Lower Rio Grande, Texas.
The Texas Journal of Science, 40(3): 259-268.

Ortmann, A. E. 1912. Notes on the Families and Genera of the Najades. Annuals of the
Carnegie Museum 8(2):222-365 +3 plates (18-20).

Simpson, C. T. 1914. A Descriptive Catalogue of the Naiades or Pearly Fresh-water
Mussels. Bryant Walker, Detroit, Michigan, 1540 pp.

Singley, J. A. 1893. Contributions to the Natural History of Texas. Geological Survey of
Texas, Part I, Texas Mollusca, pp. 297-342.

Smith, D. G., B. K. Lang & M. E. Gordon. 2003. Gametogenetic Cycle, Reproductive
Anatomy, and Larval Morphology of Popenaias popeii (Unionoida) from the Black River,
New Mexico. The Southwestern Naturalist, 48(3): 333-340.

Sterns, R. E. C. 1891. List of North American land and fresh-water shells received from
the U.S. Department of Agriculture, with notes and comments thereon. Proceedings
National Museum, Vol. XIV, No. 844:95-106.

Strecker, J. K. 1931. The Distribution of the Naiades or Pearly Fresh-Water Mussels of
Texas. Baylor University Museum Special Bulletin, 2:1-71.

NES at: ned.strenth@angelo.edu

TEXAS J. SCI. 56(3):23 1-236

AUGUST, 2004

PARABOLOIDS FOR

MAXIMUM SOLAR ENERGY COLLECTION
Ali R. Amir-Moez

Department of Mathematics
Texas Tech University
Lubbock, Texas 79409

Abstract.— Paraboloids of revolution have been used for many purposes such as
searchlights, radars and other operations concentrating on the broadcasting of waves. This
article is a study of some variations of these ideas.

1. Parabolas.- Let F(0,p) by the focus of y = -p the directrix of the
parabola x2 — 4py (Fig. 1). It is well-known that the tangent line
PT to the parabola at any point P is the bisector of the angle
between PF and PH, the perpendicular from P to the directrix.
This implies that the normal of P, PN, is the bisector of the
corresponding supplement angle (Fig. 2). This idea suggests that
some parabolic surfaces are useful in collecting solar energy. A
few samples will be given.

Fig. 2

232

THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 3, 2004

2. Paraboloid of revolution. -Rotating a parabola about its axis, one

obtains a paraboloid of revolution (Fig. 3). Since any plane
containing the axis of rotation intersects the paraboloid in a
parabola of the same size as the original one, the paraboloid has
a single focus F. Thus F collects the maximum amount of energy
when the rays are parallel to the axis. Indeed, this is quite well
known and will not be further elaborated here.

Fig. 3

3. Elliptic Paraboloids. -Consider a concave mirror of elliptic
paraboloid shape. The equation of the corresponding surface can
be chosen to be

where a and b are positive real numbers and we may choose a >
b (Fig. 4). Consider a plane containing the z-axis. This plane
intersects the xy-plane in a line. Choose an axis Ot on this line.
Let

(l,m)= (cos a, sin a), 0<a<n

be the set of direction cosines of Ot. It is clear that this will give
all possibilities of the intersection of the tz- plane with the parabo¬
loid,

AMIR-MOEZ

233

Fig. 4

as follows:

x-lt

y-mt

V2 l,2

z- — +—J2+m2=\
a2 b 2

One obtains

b2l2+a2m2 2
z= - 1

a2b2

(1)

(2)

which is a parabola in rz-plane (Fig. 4).

_x2

Note that ( l,m ) = (1,0) corresponds to z = «2and ( l,m ) = (0,1)
corresponds to z =“i2.

In general the focus of the parabola is at

2l 2

(0,0,-

a b

4(b2l2+a2m z)

)

In particular one observes that

F,=(0,oA also F2=(0,0,^)
4 4

234

THE TEXAS JOURNAL OF SCIENCE- VOL. 56, NO. 3, 2004

are respectively the foci of

x2 j y2
z- — also z-—.

a 2 b 2

Note that

b 2 < a2b2 < a 2

4 4 (b2l2+a2m2) 4

(3)

Indeed (3) shows that the line segment FXF2 extracts the maximum
energy.

4. Parabolic tubes.— Consider a parabolic cylinder (Fig. 5). Let the
equation of this cylinder be

z-ax 2, a> 0.

One can easily see that there is a line of foci whose equations are

x=0, z=— .

Indeed a concave mirror of this shape is able to collect enough
energy that one can cook a shish kabob or roast hot dogs in the
line of the foci.

AMIR-MOEZ

235

A parabolic cylinder is the simplest parabolic tube. One may
study other tubes which collect more energy. Two interesting
ones shall be studied.

Consider the parabola

y= — ( x2-b 2).
2b

Rotating this parabola about the x-axis, one obtains

4 b2

Fig. 6

It is clear that every plane that contains the x-axis intersects this
surface in a parabola whose focus is the origin (Fig. 6). Thus a
portion of this surface may be used as a concave mirror for
collecting energy.

Now rotating the parabola about a line perpendicular to its axis
which does not pass through the focus, one obtains another tube.
Consider the parabola

y-a(x2-b 2),a*^—,a > 0 ,b > 0.
2b

236

THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 3, 2004

Let the focus be at (0,q). Now we rotate the parabola about the x-
axis. A portion of this surface may be made into a concave
mirror. If q > 0, then we obtain a circular locus of foci which
arches downward (Fig. 7), while if q < 0, one obtains a circular
arc of foci bending upwards (Fig. 8). In this latter case one can
collect the maximum amount of energy from rays along this con¬
cave arc.

Acknowledgments

Both the author and the Editorial Staff wish to thank David Cecil of
TAMU-Kingsville for his review and suggestions relative to the
publishing of this manuscript.

Literature Cited

Lockwood, E. H. 1961 . A Book of Curves. Cambridge at the University Press, Cambridge,
U.K. ,199 pp.

TEXAS J. SCI. 56(3):237-252

AUGUST, 2004

CHARACTERISTICS OF PERIPHERAL POPULATIONS
OF PARTHENOGENETIC CNEM1DOPHORUS LAREDOENSIS A
(SQUAMATA: TEIIDAE), IN SOUTHERN TEXAS

James M. Walker, James E. Cordes
and Mark A. Paulissen

Department of Biological Sciences, University of Arkansas ,

Fayetteville, Arkansas 72701,

Division of Sciences, Louisiana State University at Eunice
Eunice, Louisiana 70535 and
Department of Biological and Environmental Sciences
McNeese State University, Lake Charles, Louisiana 70609

Abstract. — From 1984-2004 the distributional ecology of the parthenogenetic Cnemi-
dophorus laredoensis ( = Aspidoscelis laredoensis) complex both north and south of the Rio
Grande between Amistad Reservoir and the Gulf of Mexico was studied. Although dozens
of sites inhabited by clonal complex A of C. laredoensis were discovered within a few km
of the river (over a geographic range in parts of Webb, Zapata, Starr and Hidalgo counties,
Texas, and Tamaulipas State, Mexico), the species was observed at only three sites in two
Texas counties that were widely removed and apparently disjunct from the river-centered
zone. In order to better understand what factors limit the distribution of C. laredoensis A,
these three most distant sites from the Rio Grande (55.5 to 75.5 km) where this hybrid-
derived species is in syntopy with maternal progenitor C. gularis ( = Aspidoscelis gularis) :
Catarina, Dimmit County, and Encinal and Artesia Wells, La Salle County, Texas were
studied. Each peripheral site was characterized by sandy substrate that is known to be one
of the most important requirements for C. laredoensis A. The relative amounts of the
original thorn scrub vegetation favorable to C. gularis and chronically disturbed habitat
favorable to C. laredoensis A at each site constituted the major determinant of the relative
size of populations of the two species. The absence of C. laredoensis A north of these sites
in Dimmit and La Salle counties is probably a result of ecological resistance to expansion
consisting of unsuitable substrate and vegetation. There was no evidence that a low
frequency of hybridization between normally parthenogenetic females of C. laredoensis A
and males of C. gularis or periodic collection of C. laredoensis A at Catarina and Artesia
Wells measurably destabilized these populations.

The hypothesis that diploid parthenogenetic Cnemidophorus laredoen¬
sis (McKinney et al. [1973]; = Aspidoscelis laredoensis sensu Reeder
et al. [2002]; Sauria: Teiidae), represents the descendants of one hybrid
female between the gonochoristic species C. gularis and C. sexlineatus
( = Aspidoscelis gularis and A. sexlineata respectively, sensu Reeder et
al. [2002]) has received support from electrophoretic studies (McKinney
et al. 1973; Parker et al. 1989; Dessauer & Cole 1989), mitochondrial
DNA analysis (Wright et al. 1983), and skin histocompatibility experi¬
ments (Abuhteba 1990; Abuhteba et al. 2000; 2001). This mode of
origin for clonal complex A of C. laredoensis necessitated an improba-

238

THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 3, 2004

Figure 1. Map of Texas and position (line) of the counties (top Z = Zavala, D = Dimmit,
L = La Salle, W = Webb, Z = Zapata, S = Starr and H = Hidalgo), Rio Grande, and
state in Mexico (T = Tamaulipas) referenced in this paper. Cnemidophorus gularis
occurs in suitable habitats throughout the enlarged area, C. laredoensis A occurs in
habitats in the immediate vicinity of the river in Webb, Zapata, Starr and Hidalgo
counties and Tamaulipas and at outlying sites in Dimmit (open circle = Catarina), La
Salle (upper circle = Artesia Wells and Lower circle = Encinal), and Starr (site marked
by circle is not likely disjunct from the distribution of the species in the valley) counties,
and C. sexlineatus is limited to parts of Dimmit, Webb (where marginal syntopy occurs
with C. laredoensis A) and Starr counties.

ble sequence of events involving a single ancestral hybrid female: (1)
its growth to adulthood in syntopy with both parental species; (2) initial
avoidance of back crossing with C. gularis and C. sexlineatus ; and (3)
presence of cytogenetic determinants for production of eggs with parthe-
nogenetic potential. Success of C. laredoensis A became possible when
the descendants of the original hybrid completed fixation of partheno¬
genesis in successive generations and the incipient species “captured a
habitat” (Wright & Lowe 1968).

The geographic range of C. laredoensis A is situated between the
southern edge of the range of its paternal progenitor C. sexlineatus and
the Rio Grande in parts of Webb (only known sites of syntopy are listed
by Walker et al. 2001), Dimmit, La Salle, Zapata, Starr and Hidalgo
counties, Texas, USA, and the riverine zone bordering Mexico from
Nuevo Laredo southeast to Nuevo Progreso, Tamaulipas, Mexico (Fig.
1; see also Walker 1987a; 1987c; Walker et al. 1990; Paulissen &
Walker 1998). Remarkably, unlike its largely allopatric relationship to
C. sexlineatus , the entire range of C. laredoensis A has developed
within a small part of the vast binational distributional area of its

WALKER, CORDES & PAULISSEN

239

maternal progenitor C. gularis (Conant & Collins, 1998).

Despite extensive searching during over 50 expeditions from 1984-
2004 involving both sides of the Rio Grande between Amistad Reservoir
and the Gulf of Mexico, populations of C. laredoensis A have never
been located more than about 80 km N or a few km S of the river
(Walker 1987a; 1987c; Walker et al. 1990). In fact, all except three of
the 51 sites discovered for this parthenogen were either located within
16 km N (n = 35) and 10 km S (n = 1 1) of the river or were apparent¬
ly contiguous with this zone (n = 2 sites in Starr County). The other
three are the most distant sites from the Rio Grande known for C.
laredoensis A at 55.5 to 75.5 km to the north in Catarina, Dimmit
County, and Encinal and Artesia Wells, La Salle County, Texas (Fig.
1). Several collecting trips were made to these peripheral sites inhabited
by C. laredoensis A between 1986 and 2000 allowing (1) description of
the habitat and substrate characteristics that affect whiptail lizards at
each site; (2) estimation of the relative abundance of the parthenogen
and C. gularis and characterization of the nature of syntopy between
these species; (3) gauging of the impact of interspecific hybridization on
both species at Artesia Wells and Catarina; and (4) estimation of the
impact of collecting on populations of both species at each site. In this
paper, the data obtained on these trips are used to identify the factors
which may limit the distribution of C. laredoensis A in areas removed
from the Rio Grande.

Materials and Methods

The capture of a single individual of C. laredoensis A in September
1985 at Encinal, La Salle County, approximately 56 km from the Rio
Grande, was the first indication that the species inhabited areas well
removed from the river. Subsequently, JMW led a number of sanc¬
tioned collecting trips to explore surrounding areas of La Salle, Dimmit
and southern Zavala counties in search of the parthenogen (Walker
1987a). Sites at Catarina, Valley Wells, Asherton, Carrizo Springs and
3.2 km southwest of Carrizo Springs in Dimmit County, sites at Artesia
Wells, Cotulla, Gardendale and Millet in La Salle County, and two sites
at Crystal City in southern Zavala County were explored (Walker 1987a;
1987c). Each site was systematically searched by three or more collec¬
tors and an attempt was made to collect all lizards seen with air guns;
on average, about one in three lizards observed was captured. Collec¬
tions were made between 0900 and 1700 CDT on clear to partly cloudy
days in spring and summer during the peak period of whiptail lizard
activity; visits were also made to some sites in September and October
(Table 1).

240

THE TEXAS JOURNAL OF SCIENCE- VOL. 56, NO. 3,

2004

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242

THE TEXAS JOURNAL OF SCIENCE— VOL. 56, NO. 3, 2004

In addition to the Encinal site among those listed above, C. laredo-
ensis A was discovered only at Catarina and Artesia Wells, where it was
syntopic with maternal progenitor C. gularis. Searches for whiptail
lizards between Encinal, Artesia Wells and Catarina (and between the
other sites in Dimmit, La Salle and Zavala counties listed) produced
only specimens of the ubiquitous lizard C. gularis, plus numerous C.
sexlineatus at 3.2 km southwest of Carrizo Springs. The populations of
C. laredoensis A at Catarina, Artesia Wells, and Encinal are not only
disjunct from each other, they are also separated from the principal
distribution area of the species in the Rio Grande Valley and one area
in Starr County likely contiguous to the valley. Some of the specimens
of C. laredoensis A and C. gularis from Catarina, Encinal and Artesia
Wells reported in this paper were also used in previous studies (Walker
1987a; 1987c; Walker et al. 1989; Abuhteba 1990; 2000; 2001; Walker
et al. 1991; Paulissen et al. 1992). Specimens referenced in Table 1 are
deposited in the University of Arkansas Department of Zoology (UADZ)
and American Museum of Natural History (AMNH) collections.

Relative abundances of C. laredoensis A versus C. gularis were
determined by comparing the numbers of each species caught at each
site. The possibility that hybridization between C. laredoensis A and
C. gularis at Catarina and Artesia Wells might limit both species by
“wastage of gametes” was evaluated by tracking the number of hybrids
captured during each collecting trip and comparing it to the relative
numbers of the parental forms subsequently captured for evidence of a
decline in their numbers. Finally, the impact of repeated collections on
the population of C. laredoensis A at each site was gauged by totaling
the number of lizards captured during each collecting trip and checking
for a trend in declining numbers.

The habitat and substrate characteristics of each site were described
following the methods of Walker (1987a; see also Walker 1987c;
Paulissen et al. 2001). In brief, the relative amounts of undisturbed
thorn scrub habitat (characterized by mesquite and/or huisache trees,
scattered groundcover of a few bunchgrasses and prickly pear cactus,
and a variety of small shrubs) and disturbed habitat (characterized by
few trees and more abundant bunchgrass, low weeds, Russian thistle
with numerous open patches, trails or roads running through) were
estimated. The predominant substrate type (sand, loam or gravel) was
also recorded. The nature of the habitat disturbance was also character¬
ized as “catastrophic” if the site had been completely bulldozed and left

WALKER, CORDES & PAULISSEN

243

Figure 2. Photograph made in September 1996 showing part of the chronically disturbed site
at Artesia Wells (L-2), La Salle County, Texas, inhabited by Cnemidophorus laredoensis
A and C. gularis (note sparsely vegetated area in foreground with deep sandy soil, patch
of mesquite on the left side of the road, and buffelgrass on the upper side of the road.

to recover on its own, as “chronic” if the site was intact but subjected
to constant minor disturbance in the form of human or animal traffic,
small scale agriculture or small scale clearing of brush (Fig. 2; Table 2).

Results and Discussion

Characteristics of peripheral sites inhabited by Cnemidophorus
laredoensis A— In 1 1 visits to Catarina between 1986 and 1996 (Fig. 1),
individuals of C. laredoensis A were located between sandy roadsides
and mesquite-grass/weed associations ( n = 8), in a vacant lot among
grasses/ weeds and scattered shrubs ( n = 4) and in a trampled, over-
grazed horse pasture ( n — 68) (Table 1). The horse pasture is an
approximately 4.25 acre rectangle (135 m by 137 m less a 21 m by 62
m part surrounding a house at the northwest corner) with intermittent
thick growths of mesquite, scattered clumps of cacti, a weedy composite
and deep sandy soil, characteristics that epitomized the type of habitat
most successfully exploited by C. laredoensis A in the Rio Grande
Valley (Table 2). As many whiptails as possible were collected from the
horse pasture on each visit from 29 May 1986 through 9 September

244

THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 3, 2004

1996 (C. laredoensis A, n = 68; C. gularis , n = 16; C. laredoensis A
x C. gularis hybrids, n = 7). Cnemidop horns laredoensis A was both
more generally distributed and numerically dominant compared with C.
gularis in the chronically disturbed horse pasture throughout the study
(Paulissen et al. [2001] listed the two species as equally abundant based
on two visits in 2000; but this result was based on data taken on one trip
when weather conditions were suboptimal for lizard activity) . Although
the possibility of finding individuals of C. gularis was enhanced by
working in a border of mesquite trees along the north side of the horse
pasture, occasional individuals of this species were also encountered
elsewhere in the pasture. Areas outside of the pasture at Catarina were
much less abundantly inhabited by C. laredoensis A and C. gularis ( n
= 8) and were apparently devoid of hybrids. The Catarina site was most
recently visited by JEC on 4 June 2003 where the habitat previously
described had remained intact.

At Artesia Wells (Fig. 1, 2), individuals of C. laredoensis A were
collected and observed in the following open- structured grass/weed-
mesquite associations: sandy roadsides (n = 6); in trampled, over-grazed
cattle pens with cacti ( n = 3); in the edge of cultivated areas ( n = 2);
and near human habitations (n = 10). The relatively low numbers of
individuals of both C. laredoensis A and C. gularis collected/observed
was due to the patchy/fragmented structure of the available habitat for
whiptail lizards dispersed within an area of about six acres. The
increased numbers of C. laredoensis A collected/observed at Artesia
Wells in September 1996 compared with other visits (Table 1) resulted
from a decision to collect within a few meters of human habitations
which were avoided on previous occasions. Cnemidop horns gularis was
mostly absent from such microhabitats and it was generally encountered
in less disturbed areas of thorn scrub habitat near unpaved roads.

Encinal was the first site beyond the immediate vicinity of the Rio
Grande where C. laredoensis was discovered (Fig. 1). The collection
of a single specimen of this species (UADZ 1376) on 8 September 1985
at Encinal (in a weedy fence row north of Texas Flwy. 44 and east of
a paved road paralleling railroad tracks) was a major breakthrough in
understanding the distribution of the species north of the Rio Grande.
Two days earlier (6 September 1985), JMW counted about 25 individu¬
als of C. gularis , but did not observe C. laredoensis A, in a 5 m by 45
m strip of habitat with scattered shrubs and closely spaced bunchgrasses
on the opposite side of the highway near the railroad. All other

WALKER, CORDES & PAULISSEN

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245

Table 2. Habitat characteristics of the three peripheral sites north of the Rio Grande known to be inhabited by the allodiploid parthenogenetic
species Cnemidophorus laredoensis A (C. gularis was present and C. sexlineatus was absent at all sites). Site Codes follow Walker (1987a).

246

THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 3, 2004

individuals of C. laredoensis A collected or observed at Encinal were
syntopic with C. gularis either immediately west of main street near a
patch of sand spilled from railroad cars that had become interspersed
with grasses/weeds on both sides of railroad tracks ( n = 2) or in an
adjacent weedy lot (n = 1 + several observed). The small number of
C. laredoensis A observed at Encinal during the study were in patches
of habitat within an area of about two acres (Table 2). The large
number of C. gularis at parts of this site can be attributed to the initial
migration of individuals from relatively undisturbed thorn scrub forma¬
tions nearby into the altered grassy habitat in railroad-right-of-ways that
typically are not preferred by C. laredoensis A.

Characteristics of peripheral sites not inhabited by C. laredoensis
A— Many unsuccessful searches for C. laredoensis A have been con¬
ducted in La Salle County north of Artesia Wells along 1-35 (at Cotulla,
Gardendale and Millett), in Dimmit County at sites other than Catarina
(e.g., Valley Wells, Asherton, Carrizo Springs and SW of Carrizo
Springs) and in parts of Zavala County (vicinity of Crystal City) (Fig.
1). The presence of C. gularis and absence of C. laredoensis at the
Cotulla, Crystal City, Asherton and Carrizo Springs study sites is cor¬
related with the habitat characteristics of gravelly (not sandy) substrate
and relatively undisturbed thorn scrub vegetation. Gardendale, Millett,
and 3.2 km SW of Carrizo Springs initially seemed suitable for habita¬
tion by C. laredoensis A based on the presence of deep sandy soil,
although only the latter site closely duplicated the chronically disturbed
vegetation structures found at Artesia Wells and Catarina. Only C.
gularis was recorded on three visits to Gardendale and during two visits
to Millett.

The site at 3.2 km SW of Carrizo Springs near FM 2644 inhabited by
whiptail lizards comprised approximately five acres with sandy soil,
large clumps of cacti, scattered mesquites and sparse ground cover of
grasses/weeds that had been heavily trampled, trailed and grazed by
cattle. Although this habitat type and pattern of chronic disturbance
seemed ideal for C. laredoensis A, it was the parthenogen’s paternal
progenitor Cnemidophorus sexlineatus that was the most abundant whip-
tail lizard at the site (n — 25 + 10 observed); relatively few C. gularis
(n = 9 + 5 observed) were present (Table 1).

The conclusion that neither C. laredoensis A nor C. sexlineatus were
broadly distributed in La Salle and Dimmit counties was also supported

WALKER, CORDES & PAULISSEN

247

by information pertaining to the 15, 200 acre Chaparral Wildlife
Management Area provided by C. Ruthven (pers. comm.). This area
is located 12.8 km west of Artesia Wells on Texas FM 133 in parts of
both counties. Ruthven stated that since 1996 the Chaparral WMA staff
had been sampling herpetofauna with drift fence arrays (totaling over
3900 drift fence days). They found that Cnemidophorus gularis is very
common on the area (1,147 captures), C. sexlineatus is very rare (18
captures), but C. laredoensis A is absent.

Role of habitat and substrate characteristics in limiting C. laredoensis
A . — The three sites in Dimmit and La Salle counties where C. laredo¬
ensis A has been found away from the Rio Grande are characterized by
sandy soil and chronic to catastrophic habitat disturbance (e.g., Fig 2).
Most of the other sites in these counties lacked either one of both of
these critical habitat characteristics and so it is not surprising that C.
laredoensis A did not occur at them. Further north, the substrate
becomes generally less sandy; this combined with an more or less
unbroken expanse of undisturbed thorn scrub habitat suggests that C.
laredoensis A is unlikely to be found much further north than the
Dimmit and La Salle county sites documented in this paper.

Potential role of interspecific hybridization with C. gularis— Indi¬
viduals of C. laredoensis A and C. gularis were occasionally observed
in the same field of vision at Catarina and Artesia Wells and copulation
between the two species was observed in the horse pasture at Catarina
(Walker et al. 1991). That such copulations can lead to fertilization of
the unreduced 2n = 46 eggs of normally parthenogenetic C. laredoensis
A by the In = 23 sperm of C. gularis is indicated by the presence of
hybrids of both sexes among the lizards obtained at Catarina and Artesia
Wells.

The seven C. laredoensis x C. gularis hybrids from Catarina were
identified as follows: five males based on morphological characters and
erythrocyte nuclear diameters (UADZ 1944, snout vent length = SVL
65 mm; 1945, SVL 62 mm; 1946, SVL 66 mm; 2987, SVL 78 mm;
3506, SVL 62 mm); one subadult female based on erythrocyte nuclear
diameters (UADZ 2975, SVL 55 mm); and one female based on skin
histocompatibility experiments and triploid chromosome complement
(UADZ 3541, SVL 74 mm). Confirmed hybrids constituted only 6.4%
of all whiptails obtained at Catarina. The hybrid males were readily
identifiable based on a dorsal pattern closely resembling C. laredoensis

248

THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 3, 2004

A, ventral colors resembling C. gularis, low numbers of granules
around midbody, and postantebrachial scales of intermediate size be¬
tween the two parental species. That two females obtained at Catarina
initially appeared to be individuals of C. laredoensis A based on color
pattern, but were subsequently found to be hybrids based on other
techniques, indicates that some female C. laredoensis A x C. gularis
hybrids from this and other sites are not identifiable by external mor¬
phology. The most apparent meristic consequence of hybridization
between the two species at Catarina was a reduction in the number of
granules around midbody (mean 85.6, range 82-87, n = 7) in the
confirmed hybrids.

Two C. laredoensis x C. gularis hybrids were collected at Artesia
Wells, one male (UADZ 1626, SVL 69 mm) and one female (UADZ
2017, SVL 88 mm). The hybrid male was similar in color pattern to the
five hybrid males from Catarina. The hybrid female resembled indi¬
viduals of C. laredoensis A from Artesia Wells in dorsal pattern;
however, it exceeded the maximum SVL of 80 mm for the species at the
site and had a red-pink throat and remarkable purple-blue chest and
abdomen resembling adult males of C. gularis. Erythrocyte nuclear
diameters confirmed the hybrid status of both specimens.

Theoretically, fertilization of normally parthenogenetic females of C.
laredoensis A by males of C. gularis could destabilize the parthenogen
by reducing successful reproduction at sites such as Artesia Wells and
Catarina (Cuellar 1977). To date, this outcome has not been docu¬
mented for any pair of species of Cnemidop horns . At Catarina, seven
hybrids were conclusively identified and an additional 10 specimens
were putatively identified to C. laredoensis A (SVLs 44-71 mm) with
such low numbers of granules around midbody (mean 85.8, range 83-
88) as to arouse suspicion that they might also be hybrids (UADZ 1650
[24 May 1986]; 2733 [8 October 1987]; 2965, 2966, 2969, 2974, 2983,
2986 [13 May 1988]; 3544 [19 May 1989]; 3707 [31 July 1989]). Even
if all these individuals are hybrids, the fact that so few have been col¬
lected over the span of four years, combined with the fact that the size
of the C. laredoensis A population has shown no sign of declining (see
below and Table 3), suggests that interspecific hybridization of C.
laredoensis A with C. gularis is not an important factor affecting the
population of the parthenogen at Catarina. Presumably the same is true
at Artesia Wells.

WALKER, CORDES & PAULISSEN

249

Table 3. Summary of collecting success of each species and at the three peripheral sites
inhabited by Cnemidophorus laredoensis A, C. gularis and hybrids in Dimmit and La
Salle counties, Texas.

Site (Visits)

C. laredoensis A

C. gularis

Hybrids

Catarina (D-3, 11 visits)
Captured/Observed
Collected per visit

80/210 (38.0%)

7.3

24/44 (54.5%)

2.2

7/8 (87.5%)
0.6

Artesia Wells (L-2, 6 visits)
Captured/Observed
Collected per visit

21/39 (53.8%)

3.5

18/22 (81.8%)

2.0

2/2 (100%)
0.3

Encinal (L-3, 3 visits)
Captured/observed
Collected per visit

4/7 (57.1%)

1.3

6/40 (15.0%)

2.0

None

Totals (20 visits)
Captured/Observed
Collected per visit

105/256 (41.0%)
5.2

48/104 (46.1%)

2.4

9/10 (90.0%)
0.5

Impact of periodic collections. — Collecting trips to Catarina and
Artesia Wells made over the span of several years allowed determination
if removal of lizards had any effect on abundance of C. laredoensis A
(or C. gularis). The fact that the number of lizards captured per trip
does not show a decline from the first collecting trip to the last (Table
1) suggests that periodic collecting had no measurable impact on popula¬
tions of either species. Negative impact of collecting on each population
was mitigated by the infrequency of removal of individuals between
1985 and 1997 and escape behaviors of the species which reduced the
effectiveness of all methods of collection. The yield (% of lizards
observed that were collected per site) ranged from 38.0% at Catarina to
57.1% at Encinal for C. laredoensis A and from 15.0% at Encinal to
81.8% at Artesia Wells for C. gularis using air guns, large rubber bands
and nooses (Table 3). Each of these methods was ineffective for col¬
lection of hatchlings of C. laredoensis A (Table 1, see 8 October 1987
and 31 July 1989 results). Overall, C. laredoensis A was the most
abundant lizard at Catarina, C. gularis was the most abundant species
at Encinal, and these two species were roughly equally abundant at
Artesia Wells (Tables 1, 3).

Conclusions.— Cnemidophorus laredoensis A is one of the most
abundant vertebrates at many sites within its restricted range in southern
Texas and Tamaulipas. The ancestor of this parthenogenetic species
originated at a site inhabited by C. gularis and C. sexlineatus , possibly
either in northern Webb County, the only point of syntopy presently

250

THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 3, 2004

known for all three species, or in northern Starr County, where the
ranges of C. laredoensis A and C. sexlineatus are separated by about 30
km and C. gularis occurs throughout the area. The 10-50 km wide
separation of the ranges of C. laredoensis A from C. sexlineatus
(extending from northern Webb County through Zapata, Starr and
Hidalgo counties) is probably not a result of competitive exclusion of
one species by the other. In the absence of major geographic barriers
to the northward expansion of C. laredoensis A toward the range of G
sexlineatus and the southward expansion of C. sexlineatus toward the
Rio Grande, it appears that both are hampered by subtle ecological
barriers to expansion (i.e., substrate and/or vegetation structure). It is
possible that C laredoensis A has been able to expand more rapidly
along both sides of the Rio Grande in a zone of frequent habitat
disturbance (that may temporarily displace C. gularis) than northward
from the river through more stable habitats (inhabited by C. gularis)
toward the southern range limits of C. sexlineatus. Although both C.
laredoensis A and C. sexlineatus are sand-loving species, the former is
mostly limited to alluvial deposits (Walker 1987a) whereas the latter is
mostly limited to broadly distributed eolian deposits where species of the
lizard genus Holbrookia and the sandbur genus Cenchrus are ecological
indicators (Paulissen et al. 1997). To rephrase the question posed by
Paulissen et al. (1992) “Can parthenogenetic Cnemidop horns laredoensis
(Teiidae) coexist with its bisexual (progenitors)?” the answer in the case
of C. sexlineatus , broadly speaking, is no; the answer in the case of C.
gularis is emphatically yes.

Broad syntopy between C. laredoensis A and maternal progenitor C.
gularis within the range of the former in areas of Texas and Mexico
stems from one of two conditions. Syntopic contacts at sites such as
Encinal, Artesia Wells and Catarina could involve a temporal dynamic
in which one species is eventually excluded from the site by the inter¬
play between interspecific competition and habitat characteristics. A
stronger possibility is that syntopy is maintained through mitigation of
these effects by a variety of responses (e.g., microhabitat selection,
reproductive adaptations, tolerance of diet niche overlap and/or relaxed
selection pressure in disturbed habitats: Paulissen et al. 1992; Paulissen
2001). That habitat structure and history of land use are crucial compo¬
nents in the complex syntopic relationship between C. laredoensis A and
G gularis at particular sites (Walker 1987a; 1987b; 1987c) is consistent
with observations on these species at Encinal, Artesia Wells and
Catarina. At each site, the amounts of relatively undisturbed thorn scrub

WALKER, CORDES & PAULISSEN

251

vegetation favorable to C. gularis versus disturbed habitats favorable to
C. laredoensis A constitute the major determinants in the relative size
of populations of the two species (Tables 1, 2, 3). Catastrophic altera¬
tion of any of these sites would be expected to result in the reduction or
exclusion of C. gularis and rapid repopulation by C. laredoensis A
(Walker 1987b), whereas restoration of the original thorn scrub habitat
would likely lead to the reverse of this outcome.

Acknowledgments

Specimens of Cnemidophorus employed in this study were collected
under the terms of yearly permits issued to each of us by Texas Parks
and Wildlife. Assistance in the field was provided by Ramadan M.
Abuhteba, University of Arkansas, and Stanley E. Trauth, Arkansas
State University. C. Ruthven, Assistant Area Manager, Chaparral
Wildlife Management Area, La Salle and Dimmit counties, kindly
supplied information on Cnemidophorus studies conducted by him and
others on this area in Texas.

Literature Cited

Abuhteba, R. M. 1990. Clonal diversity in the parthenogenetic whiptail lizard,
Cnemidophorus ‘laredoensis’ complex (Sauria: Teiidae), as determined by skin
transplantation and karyological techniques. Unpubl. Ph. D. Diss., Univ. Arkansas,
Fayetteville., 82 pp.

Abuhteba, R. M., J. M. Walker & J. E. Cordes. 2000. Genetic homogeneity based on skin
histocompatibility and the evolution and systematics of parthenogenetic Cnemidophorus
laredoensis (Sauria: Teiidae). Can. J. Zool., 78:895-904.

Abuhteba, R. M., J. M. Walker & J. E. Cordes. 2001. Histoincompatibility between clonal
complexes A and B of parthenogenetic Cnemidophorus laredoensis : evidence of separate
hybrid origins. Copeia, 2001:262-266.

Conant, R. & J. T. Collins. 1998. A field guide to reptiles and amphibians of eastern and
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616 pp.

Cuellar, O. 1977. Animal parthenogenesis. Science, 197:837-843.

Dessauer, H. C. & C. J. Cole. 1989. Diversity between and within nominal forms of
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McKinney, C. O., F. R. Kay & R. A. Anderson. 1973. A new all-female species of the
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Parker, E. D., Jr., J. M. Walker & M. A. Paulissen. 1989. Clonal diversity in
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Paulissen, M. A. 2001. Ecology and behavior of lizards of the parthenogenetic

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Cnemidophorus laredoensis complex and their gonochoristic relative Cnemidophorus
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Paulissen, M. A., J. M. Walker & J. E. Cordes. 1992. Can parthenogenetic
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Paulissen, M. A., J. M. Walker & J. E. Cordes. 1997. Diet of the Texas yellow-faced
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Paulissen, M. A., J. M. Walker & J. E. Cordes. 2001. Status of the parthenogenetic
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Reeder, T. W., C. J. Cole & H. C. Dessauer. 2002. Phylogenetic relationships of whiptail
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MAP at: mpauliss@mail.mcneese.edu

TEXAS J. SCI. 56(3):253-262

AUGUST, 2004

COMPARISON OF BRANCH ELONGATION
AMONG FOUR ACACIA SPECIES AND TEXAS EBONY IN
THE LOWER RIO GRANDE VALLEY OF TEXAS

Melissa R. Eddy and Frank W. Judd

Department of Biology, University of Texas-Pan American
Edinburg, Texas 78541-2999

Abstract.— Branch elongation was compared among four Acacia species ( Acacia
berlandieri , A.farnesiana, A. rigidula , A. schaffneri ) and Texas ebony ( Chloroleucon ebano)
at three sites in Hidalgo and Starr counties, Texas. Most of the branch elongation occurred
in fall and early winter in A. berlandieri , A. farnesiana and A. rigidula, but in A. schaffneri
most of the growth occurred in late winter and spring. Branch elongation in Texas ebony
was not concentrated in a given season. Acacia berlandieri, A. farnesiana and A. rigidula
had significant positive correlations between branch elongation and rainfall, but A. schaffneri
and Texas ebony did not. Variation in branch elongation among Acacia species is as great
as that which occurs between the Acacia species and Texas ebony.

Phenological studies are important because they provide descriptive
information essential to the elucidation of reproductive and growth
patterns. Such studies are a crucial prelude to formulation of hypotheses
in experimental investigations (Bullock & Solis-Magallanes 1990; Eddy
& Judd 2003). There have been only two studies (Vora 1990; Eddy &
Judd 2003) of the phenology of woody plants in the Lower Rio Grande
Valley of Texas (LRGV). Vora (1990) reported on flowering, fruiting,
leaf growth and leaf drop of 19 native species (most were woody)
occurring primarily at Santa Ana National Wildlife Refuge, 12.1 km
south of Alamo, Hidalgo County, Texas. He did not quantitatively
analyze comparisons among species in the characteristics he examined,
and he did not quantify the relationships between climatic factors and the
reproductive and vegetative responses of the species studied. Eddy &
Judd (2003) described and quantified the flowering and fruiting phenolo¬
gy of Acacia berlandieri , A. minuata (= A. farnesiana) , A . rigidula , A.
schaffneri and Chloroleucon ebano at two sites in Hidalgo County and
one site in Starr County.

The objectives of this study were to: (1) describe and quantify
patterns of branch elongation among four Acacia species (A. berlandieri ,
A. farnesiana, A. rigidula and A. schaffneri) and Chloroleucon ebano ;
(2) quantitatively examine the relationships between climatic factors and
branch elongation of the species studied; and (3) determine if the
magnitude of differences in branch elongation between members of the

254

THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 3, 2004

genus Acacia are as great as those between any of the Acacia species
and Chloroleucon ebano. The null hypotheses tested were: (1) there
are no significant differences in the patterns of branch elongation of the
Acacia species studied; (2) variation in branch elongation among the
Acacia species is less than the variation between any of the Acacia
species and Chloroleucon ebano ; and (3) there are no significant
correlations between climatic factors and branch elongation.

Materials and Methods

Study area. — The LRGV comprises the southernmost four counties of
Texas (Cameron, Hidalgo, Starr and Willacy counties). This study was
conducted in Hidalgo and Starr counties. The climate is semi-arid and
subtropical. Summers are long and hot and winters are short and mild
(Lonard et al. 1991; Eddy & Judd 2003). The mean length of the frost-
free period is 330 days, but winters often pass without a freezing
temperature. Mean monthly temperature is greater than 16°C in all
months throughout the LRGV. In summer, a temperature of 32.5 °C or
greater occurs for 116 or more days.

Mean annual rainfall ranges from a high of 71.5 cm at Harlingen,
Cameron County to a low of 54.9 cm at Rio Grande City, Starr County.
From 28 to 33 % of the annual rainfall occurs in September and October
and 65 to 73% of the annual rainfall occurs from May through October.
Most of the precipitation results from thunderstorms.

Vegetation of the study sites is brush grassland and thorn woodland
(Lonard et al. 1991; Eddy & Judd 2003). Study sites were the Castilla
Ranch (CR) 11.9 km north of Rio Grande City, Starr County, Yturria
Brush Tract (YBT) 7. 1 km west of La Joya, Hidalgo County and Santa
Ana National Wildlife Refuge (SAN) 12. 1 km south of Alamo, Hidalgo
County.

Description of species .—Acacia berlandieri (guajillo) is a semi¬
evergreen shrub ranging in height from 1.0 to 4.0 m (Lonard et al.
1991; Everitt et al. 2002; Richardson 1995). It is found on a variety of
soils, but is especially abundant in the LRGV on caliche soils in western
Hidalgo and Starr counties. The leaves are fern-like, bipinnately
compound, alternate and have 30 to 50 pairs of leaflets per pinna
(Lonard et al. 1991; Eddy & Judd 2003). The flowers are white, and
the legumes are 10.2 to 15.2 cm long with 5 to 10 dark brown seeds
(Taylor et al. 1999; Eddy & Judd 2003).

EDDY & JUDD

255

Acacia famesiana (huisache) is a small, spiny tree or shrub ranging
from 2.0 to 4.0 m tall (Lonard et al. 1991; Everitt et al. 2002; Eddy &
Judd 2003). It occurs on a variety of soil types (Lonard et al. 1991).
The leaves are bipinnately compound, alternate, with 2 to 8 pairs of
pinnae and 10 to 25 pairs of leaflets per pinna (Lonard et al. 1991).
The flowers are yellow to gold, and the fruit can be reddish brown,
purple, or black (Everitt et al. 2002). The legumes are 5.1 to 7.6 cm
long and the seeds are in 2 rows within them (Everitt et al.2002; Taylor
et al. 1999).

Acacia rigidula (black brush) is a white-spined, multiple-stemmed
shrub that grows to a maximum height of 3.0 m (Lonard et al. 1991;
Eddy & Judd 2003). It is often found with guajillo. Black brush is
found on clay or gravelly soils in the LRGV (Richardson 1995). The
leaves are alternate, bipinnately compound with 1 or 2 pairs of pinnae
and 2 to 4 leaflets per pinna (Lonard et al. 1991). The flowers are
yellowish or white. The legume is black to reddish black, 5. 1 to 8.9 cm
long, and constricted between the seeds (Richardson 1995; Taylor et al.
1999).

Acacia schaffneri (huisachillo) is a spiny, rounded shrub that grows
to a maximum height of 2.0 m (Lonard et al. 1991). It occurs on sandy
and clay soils in the LRGV (Richardson 1995). Leaves are alternate,
bipinnately compound with 2 to 5 pairs of pinnae and 10 to 15 pairs of
leaflets per pinna (Lonard et al. 1991). Flowers are yellow. The fruit
is a linear, black, pubescent legume from 4.0 to 13.0 cm long and
constricted between the seeds (Correll & Johnston 1979; Lonard et al.
1991; Everitt et al. 2002; Richardson 1995).

Chloroleucon ebano (Texas ebony) is a tree with a maximum height
of 15 m (Richardson 1995), but usually it is less than 10 m tall (Lonard
et al. 1991). It has zig-zag branches with stout stipular spines. The
leaves are alternate or fascicled and bipinnately compound with 3 to 6
pairs of leaflets per pinna. Texas ebony occurs on sandy loam soils in
the LRGV (Lonard et al. 1991). The flowers are white, and the fruit is
a thick- walled woody legume.

Field and statistical methods.— Only black brush was present at all
three study sites (Table 1). Each of the other four species was present
at two sites. SAN and YBT each had four of the five species and CR
had three species present. Ten individuals from each of the species

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THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 3, 2004

Table 1. Species present at study sites in Hidalgo and Starr counties. NWR = National
Wildlife Refuge.

Species

Castilla

Ranch

Santa Ana
NWR

Yturria Brush
Tract

Acacia berlandieri

Acacia farnesiana

Acacia rigidula

Acacia schaffneri

Chloroleucon ebano

present at a site were marked for study. Shrubs (guajillo, huisachillo
and black brush) were 1.5 m in height or taller. Huisache and Texas
ebony were 3 m or taller. Shrubs and trees of these heights were known
to be capable of possessing fruit. Distance between marked individuals
ranged from 8 m to 2,320 m. All plants selected were healthy. Plants
were marked with colored flagging and two aluminum tags bearing a
unique identification number.

Branch elongation was monitored by applying a ring of paint just
below the terminal bud on three randomly selected branches on each
individual. The distance from the paint mark to the tip of the branch
was measured to the nearest mm at monthly intervals from October 1998
through August 1999. The mean elongation of the three branches was
recorded as the shoot elongation for the individual for a given month.

Daily air temperatures, precipitation and photoperiod were obtained
from the National Climatic Data Center for McAllen, Texas. Long-term
precipitation and temperature data were obtained from the Office of the
Texas State Climatologist.

Results

Mean monthly photoperiod at McAllen, Texas ranged from 10 h and
32 min in December 1998 to 13 h and 45 min in June 1999 (Table 2).
The study sites varied from McAllen by less than 15 min latitude, so
there was little variation between photoperiod at McAllen and any of the
three study sites. Likewise, there was little variation in photoperiod
among the study sites.

Because of the distance between the study sites and the distance
between them and McAllen, it was possible that rain might have
occurred at McAllen and not at any of the study sites. Likewise, it was

EDDY & JUDD

257

Table 2. Climatic data for McAllen, Texas.

Month

Rain (cm)
1998-99

Rain (cm)
1958-98

Mean

Temp. (°C)
1998-99

Mean

Temp. (°C)
1958-98

Mean

Daylight (min)
1998-99

Sept.

24.09

11.11

28.7

29.1

738

Oct.

7.23

7.93

24.8

25.2

692

Nov.

2.61

2.82

21.6

20.6

652

Dec.

0.71

2.81

16.7

16.6

632

Jan.

0.08

3.74

18.2

15.0

643

Feb.

0.03

3.63

21.9

17.3

677

Mar.

5.74

2.02

23.0

21.1

721

Apr.

0.10

3.65

26.9

25.0

767

May

3.17

6.70

28.9

27.6

806

Jun.

1.27

7.06

30.9

29.9

825

Jul.

0.41

3.71

29.8

30.6

816

Aug.

7.82

5.51

31.2

30.9

782

possible that rain occurred at a study site and not at McAllen or that rain
occurred at one study site and not at the other two sites. Using local
observer reports it was previously shown (Eddy & Judd 2003) that there
was less than 1 .0 cm difference in monthly rainfall total of the SAN and
YBT sites in all months of this study. The CR site generally was within
1.5 cm in monthly rainfall of the other two sites, but in October 1998,
CR received 2.6 cm more rain than the other sites and in August 1999,
CR received 3.0 cm less rain than the other two sites.

Branches were first marked for monitoring growth in length in
October 1998. Consequently, November 1998 is the first month that
data on branch elongation was reported. Rainfall in October and
November 1998 was close to the long-term average for these months
(Table 2). However, rainfall in December, January and February was
92% lower than the long-term average. And, rainfall from April
through July, 1999 was 77% lower than the long-term average. Air
temperature from January through June, 1999 was markedly higher than
the 40-year average (Table 2).

Mean monthly branch elongation is shown among species, months and
sites in Table 3. Analysis of variance (ANOVA) showed significant
variation in branch elongation among months in all species (Table 4),
but there was no significant variation in branch elongation among
months in black brush at the CR site or in Texas ebony at the SAN site.

In guajillo, 63.1% of the increase in branch length occurred in
November, December and January at the YBT site and 69.1% of the
growth occurred in these same three months at the SAN site. Much of

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THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 3, 2004

Table 3. Comparison of mean branch elongation (cm) per month among months, species,
and study sites. N = 10 for each mean. Numbers in parenthesis equal one standard
error of the mean. Sp = species, A. b. — Acacia berlandieri, A. f = Acacia fames iana,
A. r. = Acacia rigidula, A. s. = Acacia schajfneri, C. e. = Chloroleucon ebano, CR
= Castilla Ranch, SAN = Santa Ana National Wildlife Refuge and YBT = Yturria
Brush Tract.

Sp &
Site

Nov

Dec

Jan

Feb

Mar

Apr

May

Jun

Jul

Aug

A. b.

3.67

1.91

1.38

0.02

0.06

0.73

0.93

1.07

0.44

0.79

YBT

(0.72)

(0.70)

(0.52)

(0.02)

(0.03)

(0.27)

(0.51)

(0.70)

(0.19)

(0.35)

A. b.

4.44

3.01

0.84

0.88

0.92

0.50

1.05

0.01

0.34

0.00

SAN

(0.58)

(1-41)

(0.52)

(0.46)

(0.55)

(0.26)

(0.62)

(0.01)

(0.34)

(0.00)

A.f

7.82

0.13

0.10

0.33

0.22

2.40

2.75

0.41

0.15

0.29

(1.01)

(0.11)

(0.07)

(0.19)

(0.16)

(1.16)

(1.32)

(0.28)

(0.15)

(0.28)

A.f

9.04

1.82

0.83

0.00

0.08

3.87

0.34

0.49

0.89

1.41

SAN

(1.69)

(1.59)

(0.45)

(0.00)

(0.08)

(1.74)

(0.16)

(0.40)

(0.71)

(1.01)

A. r.

4.45

1.73

0.12

0.64

0.49

2.14

3.92

1.19

4.83

3.20

(1.07)

(1.69)

(0.07)

(0.40)

(0.33)

(0.98)

(1.28)

(0.62)

(1.73)

(1.19)

A. r.

5.31

1.05

0.19

0.01

0.23

0.35

0.12

0.04

0.02

1.23

YBT

(0.91)

(0.42)

(0.12)

(0.01)

(0.20)

(0.19)

(0.12)

(0.04)

(0.01)

(0.88)

A. r.

4.52

1.13

0.31

0.18

2.21

0.45

1.24

0.46

1.15

SAN

(1.11)

(0.50)

(0.21)

(0.15)

(0.16)

(0.80)

(0.21)

(0.59)

(0.38)

(0.60)

A. s.

1.10

1.07

0.41

2.87

2.47

2.27

5.10

0.24

0.10

2.35

(0.51)

(0.59)

(0.25)

(1.25)

(0.69)

(0.97)

(1.47)

(0.20)

(0.06)

(1-25)

A. s.

1.34

0.00

0.34

0.86

6.95

2.78

2.93

0.15

0.06

YBT

(1.09)

(0.00)

(0.35)

(0.70)

(1.90)

(1.70)

(1.41)

(0.07)

(0.04)

(0.05)

C. e.

2.89

0.14

0.45

0.04

0.13

2.36

1.95

0.11

0.02

3.61

YBT

(0.86)

(0.09)

(0.42)

(0.04)

(0.13)

(1.01)

(0.73)

(0.09)

(0.01)

(1.61)

C. e.

0.45

1.67

0.01

0.10

0.00

1.69

0.29

0.54

0.41

0.39

SAN

(0.45)

(0.77)

(0.01)

(0.07)

(0.00)

(1.12)

(0.19)

(0.33)

(0.35)

(0.33)

the growth in branch length took place in November alone in huisache
(53.6% at the CR site and 48.2% at the SAN site). Increase in branch
length was concentrated in November and December in black brush at
two of the three sites (74.4% at the YBT site, 47.8% at the SAN site).
Branch elongation at the CR site was distributed more evenly among
months, but was low in January, February and March.

Branch elongation in huisachillo showed a very different seasonal
pattern than the other three Acacia species. At both the CR site (70.7%)
and the SAN site (87.4%) most of the growth occurred in late winter
and spring, i.e., February, March, April and May. In Texas ebony,
branch elongation was distributed at peaks throughout the ten months.
At the YBT site growth was concentrated in November, April, May and
August, while at the SAN site growth was greatest in December and
April.

EDDY & JUDD

259

Table 4. Analysis of Variance of mean monthly branch elongation among species and sites.
CR = Castilla Ranch, YBT = Yturria Brush Tract and SAN = Santa Ana National
Wildlife Refuge. DF = degrees of freedom, SS = Sums of Squares, MS = Mean
Squares, F = AN OVA value. NS = Not Significant (P > .05), * = P < .01, ** = P
< .001.

Species and Site

Source

Acacia berlandieri

Among months

99.368

11.041

39.573**

YBT

Within months

25.122

0.279

Acacia berlandieri

Among months

193.913

21.546

6.069**

SAN

Within months

319.517

3.550

Acacia farnesiana

Among months

536.198

59.575

13.680**

Within months

391.198

4.355

Acacia farnesiana

Among months

686.108

76.234

7.371**

SAN

Within months

930.789

10.342

Acacia rigidula

Among months

70.136

7.793

0.562 NS

Within months

1,247.210

13.858

Acacia rigidula

Among months

237.293

26.367

14.017**

YBT

Within months

169.315

1.881

Acacia rigidula

Among months

160.316

17.813

5.754**

SAN

Within months

278.645

3.096

Acacia schajfneri

Among months

212.858

23.651

3.192*

Within months

666.922

7.410

Acacia schajfneri

Among months

433.642

48.182

4.683**

YBT

Within months

925.927

10.288

Chloroleucon ebano

Among months

173.204

19.245

3.779**

YBT

Within months

458.286

5.092

Chloroleucon ebano

Among months

34.732

3.859

1.582 NS

SAN

Within months

219.555

2.440

Correlation between mean monthly branch elongation and the previous
month’s rainfall is compared between species and sites in Table 5. This
correlation allows time for growth after rainfall occurs. Guajillo,
huisache and black brush showed significant positive correlations at one
or two sites. Huisachillo and Texas ebony did not have significant
correlations with the previous month’s rainfall. There were no signifi¬
cant correlations in any species between mean monthly branch elonga¬
tion and mean monthly temperature. Only guajillo at the SAN site
showed a significant correlation between mean monthly branch elonga¬
tion and mean monthly photoperiod (r = -0.682, 8 df,P< 0.05).

Mean branch elongation over the 10 months of study was used to
compare growth between sites within species. Guajillo, huisache and
huisachillo did not exhibit significant variation between sites.
Conversely, black brush had significant variation among the three sites
where it was studied (F = 11.897, 2 & 27 df9 P < 0.001). The SAN

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THE TEXAS JOURNAL OF SCIENCE— VOL. 56, NO. 3, 2004

Table 5. Correlation coefficients for mean monthly branch elongation versus the previous
month’s rainfall. N = 10 for all species and locations. CR = Castilla Ranch, YBT =
Yturria Brush Tract and SAN = Santa Ana National Wildlife Refuge. NS = not
significant ( P > .05). * = P < .05, ** = P < .01.

Species

YBT

SAN

Acacia berlandieri

0.715 *

0.563 NS

Acacia farnesiana

0.739 *

0.884 **

Acacia rigidula

0.304 NS

0.688 *

0.923 **

Acacia schaffneri

- 0.324 NS

- 0.116 NS

Chloroleucon ebano

0.385 NS

0.554 NS

site had greater mean branch elongation than the YBT site (t = 2.166,
18 df, P < 0.05) and the CR site had a greater mean than either the
SAN site (t = 2.996, 18 df \ P < 0.01), or the YBT site (t = 4.050, 18
df ’ P < 0.001). Texas ebony also showed significant variation in
branch elongation between sites ( t = 2.287, 18 df, P < 0.05).

Discussion

Hypothesis 1 that there are no significant differences in the patterns
of branch elongation of the Acacia species studied was falsified. Branch
elongation occurred primarily in fall and early winter in guajillo,
huisache and black brush but in huisachillo, branch elongation prin¬
cipally took place in late winter and spring. Eddy & Judd (2003) also
found significant differences in the flowering and fruiting phenologies
of these Acacia species.

Hypothesis 2 that variation in branch elongation among the Acacia
species was less than the variation between any of the Acacia species
and Texas ebony also was falsified. Huisachillo differed from the other
species of Acacia in the timing of branch elongation (as explained
above) and unlike the other Acacia species, huisachillo did not show a
significant correlation with rainfall. It was similar to Texas ebony in
this respect. Eddy & Judd (2003) found that the flowering and fruiting
of these Acacia species were more similar to each other than to Texas
ebony. Thus, the data on branch elongation are very different from that
on flowering and fruiting.

Hypothesis 3 that there are no significant correlations between
climatic factors and branch elongation also was falsified. Guajillo,
huisache and black brush showed significant positive correlations with
rainfall. Additionally, guajillo at the SAN site had a significant inverse
correlation with mean monthly photoperiod. Thus, these findings

EDDY & JUDD

261

support the conclusion of New (1984) that growth in Acacia species is
often correlated with moisture. Vora (1990) stated that plant growth and
reproduction were keyed to rainfall and soil moisture for most of the 19
species he studied at Santa Ana National Wildlife Refuge. Also, Nilsen
& Muller (1981) found that branch elongation in the legume Lotus
scoparius in California was primarily influenced by soil moisture and
they suggested that this is a common response in chaparral plants.

These data were obtained during a drought. Rainfall from November
1998 through August 1999 in the LRGV was only about half (47.3%)
of the long-term average for this time period. Clearly, the drought may
have influenced the phenol ogical responses of the species studied.
Furthermore, it is possible that data for September and October, which
are lacking here, might have produced different conclusions about the
seasonal patterns of branch elongation since these are the two months
with the greatest rainfall in the LRGV. However, this seems unlikely
because there was no correlation between rainfall and branch elongation
in huisachillo.

Additional information, especially from wet years, is needed to
elucidate the full range of growth responses for these and other species
of Acacia in the LRGV. This study points to the need for experiments
on the effects of soil moisture on growth to help explain the differences
observed between huisachillo and the other three Acacia species.

Among sites variation is not often assessed in phenological studies. It
was shown that this was an important factor in two of the five species
studied. In arid environments, variation in soil moisture is common
both within and between sites (Beatley 1974) and it may be the proxi¬
mate cause of variation in phenological responses in this study.

Acknowledgments

This paper is part of a master’s thesis by M. Eddy submitted to the
Department of Biology at the University of Texas- Pan American.
Thanks go to D. Howell and C. Best of the United States Fish and
Wildlife Service for permits to study phenology at Santa Ana National
Wildlife Refuge. Special thanks go to D. R. Rios, Sr., D. R. Rios, Jr.,
J. Rios and C. Eddy for field assistance.

Literature Cited

Beatley, J. C. 1974. Phenological events and their environmental triggers in Mojave Desert

ecosystems. Ecology, 55(4): 856-863.

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Bullock, S. H. & J. A. Solis-Magallanes. 1990. Phenology of canopy trees of a tropical
deciduous forest in Mexico. Biotropica, 22(l):22-35.

Correll, D. S. & M. C. Johnston. 1979. Manual of the vascular plants of Texas. Texas
Research Foundation, Renner, Texas, 1881 pp.

Eddy, M. R. & F. W. Judd. 2003. Phenology of Acacia berlandieri , A. minuata, A.
rigidula, A. schqffneri, and Chloroleucon ebano in the Lower Rio Grande Valley of
Texas during a drought. Southwest. Nat., 48(3) :321 -332.

Everitt, J. H., D. L. Drawe & R. I. Lonard. 2002. Trees, shrubs, and cacti of South
Texas. Texas Tech University Press, Lubbock, 249 pp.

Lonard, R. I., J. H. Everitt & F. W. Judd. 1991. Woody plants of the Lower Rio Grande
Valley, Texas. Misc. Publications, No. 7. Texas Memorial Museum. Univ. of Texas
at Austin, 179 pp.

New, T. R. 1984. A biology of Acacias. Oxford Univ. Press, Melbourne, Australia, 153

pp.

Nilsen, E. T. & W. H. Muller. 1981. Phenology of the drought-deciduous shrub Lotus
scoparius : climatic controls and adaptive significance. Ecological Monographs, 51(3):
323-341.

Richardson, A. 1995. Plants of the Rio Grande Delta. Univ. Texas at Austin Press. 322
pp. + 94 color plates.

Taylor, R. B., J. Rutledge & J. G. Herrera. 1999. A field guide to common South Texas
shrubs. Texas Parks & Wildlife Press, Austin, 106 pp.

Vora, R. 1990. Plant phenology in the Lower Rio Grande Valley of Texas. Texas J.Sci.,
42(2): 137-142.

FWJ at: Qudd@panam.edu

TEXAS J. SCI. 56(3), AUGUST, 2004

263

GENERAL NOTES

SYSTEMATIC AND ECOLOGICAL NOTES ON
TUBIF1COIDES HETEROCHAETUS (OLIGOCHAET A : TUBIFICIDAE)
FROM THE NECHES RIVER ESTUARY, TEXAS

Richard C. Harrel

Department of Biology, Lamar University
Beaumont, Texas 77710

Tubificoides heterochaetus (Michaelsen 1926) is an estuarine oligo-
chaete in the Family Tubificidae that has been reported in Europe and
North America. North American records include Virginia, North
Carolina, Florida, Louisiana and the Sabine-Neches estuary in Texas
(Wern 1980; Shirley & Loden 1982; Harrel & Hall 1991; Milligan
1996; Harrel & Smith 2002). All of the publications concerning this
species, except Shirley & Loden (1982), are taxonomic, and no informa¬
tion is given concerning its water quality tolerance.

The taxonomic status of this species was in a state of confusion until
recently. It was originally described by Michaelsen (1926) and placed
in the genus Limnodrilus and later transferred to the genus Peloscolex
(Lastockin 1937; Cekanovskaya 1962; Brinkhurst & Jamison 1971).
Holmquist (1978) established the genus Tubificoides and in 1979
Brinkhurst & Baker transferred the marine and estuarine Peloscolex to
the genus Tubificoides .

Descriptions of T. heterochaetus in the literature vary from one author
to another and most were based on specific lectotypes and did not con¬
sider all of the morphological variation that occur in the species.
Tubificoides heterochaetus was originally described by Michaelsen
(1926) as possessing a cuticular penis sheath. Brinkhurst & Jamison
(1971) and Brinkhurst & Baker (1979) described it as lacking a penis
sheath. Baker (1981) redescribed the species to correct this. Milligan
(1996) contains the only taxonomic key, known by this author, that can
be used by an applied biologist for proper identification of T. hetero¬
chaetus. However, numbers of setae per bundle, lengths of setae, and
width and length of the penis sheath vary more than the scattered litera¬
ture states. Thus, an updated description of the species is given based
on the literature and examination of 302 specimens collected from the
Neches River estuary in Texas. The diagnostic characteristics of the

264

THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 3, 2004

genus are based on histological genitalia structures and these are not
often visible in specimens collected and prepared for ecological pur¬
poses. Thus, the description below is based on structures visible without
special handling or dissection. All specimens examined were killed and
preserved in formalin containing rose bengal stain, stored in 70 percent
ethanol and mounted in CMC- 10 media on microscope slides.

Complete specimens 5 to 9 mm long and ranged from 46 to 66
segments, but most were incomplete. Maximum width ranged from
about 375 to 500 /x,m at segment X or XI. Anterior segments (I-XII) are
non-papillate and distinctly wider than posterior papillate segments which
are 70 to 160 /xm wide (Figure 1). The posterior papillate segments are
elongate and often constricted at their base. The prostomium is conical
and shorter or equal to its base at the peristomium. Anterior segments
II through XII become progressively longer. Segments II through IX
have secondary annulations and have 3 to 8 (mostly 5 or 6) 38 to 50 /xm
long ventral and dorsal bifid setae per bundle with equal length teeth.
Segment IX may have one, two or no setae. Clitellar segments X, XI
and XII lack setae. A short thimble-shaped penis ranging from 36 to 37
/xm wide at the base and 37 to 46 /xm long with a thin cuticular sheath
may be present in or just outside of segment XI. Only eight of 302
specimens examined had a visible penis sheath; two collected in
February, two in May, one in August and three in November. Segment
XIII decreases in width from anterior to posterior and scattered papille
first appear. Segments behind XIII are covered with oblong papillae,
but the posterior segments of complete specimens had very few or
lacked papillae. Some post-clitellar segments possess 1 , 2 or occasional¬
ly 3 apparently simple pointed setae per bundle 54 to 67 /xm long.
Some posterior setae are actually bifid and the upper tooth is longer and
thicker than the shorter, thinner lower tooth, which is not visible unless
turned just right. The posterior setae are often broken, difficult to see
or absent in some segments. If all of the papillate segments of a speci¬
men are missing it could easily be misidentified as Limnodrilus.

Harrel et al. (1976), Harrel & Hall (1991) and Harrel & Smith (2002)
conducted three year-long surveys, with seasonal sampling of macro¬
benthos at the same seven collection stations in the highly industrialized,
tidal, lower Neches River. A 1971-72 study (Harrel et al. 1976) was
conducted before implementation of the Clean Water Act (CWA) when
this section of the river was listed as the second most polluted waterway
in the state with a permitted BOD (biochemical oxygen demand) waste
load of 123,125 kg/day. Oxygen depletion (concentrations <2 mg/L)

TEXAS J. SCI. 56(3), AUGUST, 2004

265

Figure 1. Tubificoides heterochaetus : (a) body, (b) tip of anterior and dorsal seta, and (c)
tip of posterior weakly bifid seta.

occurred at all stations and toxic pollutants were present in the water and
the substrate. No T. heterochaetus were collected during this survey
and they may have been excluded by the heavy load of organic and toxic
pollutants in the river.

During a 1984-85 study (Harrel & Hall 1991), after implementation
of the first two phases of the CWA and a 93 percent reduction in the
permitted BOD pollution load in the river to 8,717 kg/day, a total of
525 specimens of T. heterchaetus were collected from six of the seven
sampling stations. Density at individual collection stations ranged from
zero to 1196/m2 and maximum density occurred during February.
Salinity ranged from <0.5 ppt to 8.5 ppt at the stations and depths
where it occurred.

During a 1999 study (Harrel & Smith 2002), after implementation of
phase 3 of the CWA, but a 19 percent increase in the permitted BOD
waste load in the river, 302 specimens of T. heterochaetus were col¬
lected at five of the seven collecting stations. Density at individual
collecting stations ranged from zero to 991/m2 and maximum density
occurred in November. Salinity ranged from <0.5 ppt to 13.2 ppt.

During 1978 and 1979 Wern (1980) conducted monthly collections of
macrobenthos from 12 stations in the Keith Lake system of marsh lakes
located between the Sabine-Neches navigation channel, the Gulf of
Mexico and the Intracoastal Waterway. She collected 1254 specimens

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of T. heterochaetus and some specimens were collected at all 12 stations
at some time during the study. Density ranged from zero to 3075/m2
and highest densities occurred during July and August, which was
attributed to a reproductive event. Salinity ranged from < 0.5 to 20 ppt.
Mean station bottom water dissolved oxygen concentrations ranged from
6.0 to 7. 1 mg/L. No permitted effluents were released directly into this
system, but some contaminants (e.g., metals, oil and grease) were
present in the sediments and were probably transported in by tidal action
from the Intracoastal Waterway and the Sabine- Neches Navigation
channel or from oil field activity in the area. These occurred in higher
concentrations at some stations than at others, but no differences in
macrobenthos distribution, abundance or diversity could be attributed to
pollution.

Shirley & Loden (1982) reported T. heterochaetus from the Calcasieu
River estuary in Louisiana, which is located about 80 km east of the
Neches River and Keith Lake estuaries. Specimens were collected from
10 of 27 stations sampled during 1974 to 1976. No specimens were
collected at stations where oxygen depletion occurred and environmental
parameters where they were collected included: (1) salinity - 2.3 to 14. 1
ppt, (2) oxygen percent saturation - 68 to 1 12%, (3) depth - 1.0 to 5 m,
and (4) substrate - clay and silt. Density rarely exceeded 100/m2 and
average density was 46.2/m2.

Other Oligochaetes that occurred with T. heterochaetus in the Neches
River and Keith Lake estuaries include Limnodrilus hoffineisteri , L.
udekmianus , Ilyodrilus templetoni , Aulodrilus piguetti, A. pluriseta ,
Dero nivae, D. Jurcata, Slavinia appendiculata , Nais variabilis and
Paranais grandis. All of these are considered freshwater species, except
P. grandis which has been reported only from coastal Louisiana and
Texas. Polychates that were common where T. heterochaetus occurred
were Hobsoni grayi , Parandalia americana, Neanthes succine ,
Laeonereis culveri, Poly dor a socialis , Streblospio benedicti and
Mediomastus calif omiensis .

Tubificoides heterochaetus is a oligohaline to mesohaline estuarine
species restricted to habitats where the salinity varies from <0.5 to 20
ppt, but was uncommon where salinity was <2 ppt or > 14 ppt. It
occurred in sand, silt and clay substrates and at depths to at least five
meters. It is tolerant to moderate pollution and cannot tolerate oxygen
depletion or severe pollution. It was not collected in the Neches River
estuary until after pollution abatement occurred resulting in improved
water quality when it became a common component of the benthic
community.

TEXAS J. SCI. 56(3), AUGUST, 2004

267

Literature Cited

Baker, H. R. 1981. A redescription of Tubificoides heterochaetus (Michaelsen)
(Oligochaeta: Tubificidae). Proc. Biol. Soc. Wash., 94:564-568.

Brinkhurst, R. O. & B. G. M. Jamieson. 1971. Aquatic Oligochaeta of the world. Univ.
of Toronto Press, 860 pp.

Brinkhurst, R. O. & H. R. Baker. 1979. A review of the marine Tubificidae (Oligochaeta)
of North America. Can. J. Zool., 67:1553-1569.

Chekanovskaya, O. V. 1962. Aquatic Oligochaeta of the USSR. Translated from Russian
in 1981 by Amerind Publ. Co. Ltd., New Delhi, 513 pp.

Harrel, R. C., J. Ashcraft, R. Howard & L. Patterson. 1976. Stress and community
structure of macrobenthos in a Gulf Coast riverine estuary. Cont. Mar. Sci., 20:69-81.

Harrel, R. C. & M. A. Hall. 1991. Macrobenthic community structure before and after
pollution abatement in the Neches River estuary (Texas). Hydrobiologia, 211:241-252.

Harrel, R. C. & S. T. Smith. 2002. Macrobenthic community structure before, during, and
after implementation of the Clean Water Act in the Neches River estuary (Texas).
Hydrobiologia, 474:213-222.

Holmquist, C. 1978. Revision of the genus Peloscolex (Oligochaeta, Tubificidae). 1.
Morphological and anatomical scrutiny; with discussion on the generic level. Zool. Scr. ,
7:187-208.

Lastockin, D. A. 1937. New species of Oligochaeta limicola in the European part of the
USSR. Dokl. Akad. Nauk. SRR, 17:233-235.

Michaelsen, W. 1926. Oligochaeten aus dem. Ryck bei Greifswald und von benachbarten
Meeresgebieten. Mitt. Hamb. Zool. Mus. Inst., 42:21-29

Milligan, M. R. 1996. Identification manual for the aquatic Oligochaeta of Florida, Volume
II Estuarine and nearshore marine oligochaetes. Bureau of Water Resources Protection,
Florida Dept, of Environmental Protection, Tallahassee, 239 pp.

Shirley, T. C. & M. S. Loden. 1982. The Tubificidae (Annelia, Oligochaeta) of a
Louisiana estuary: ecology and systematics, with the description of a new species.
Estuaries, 5:47-56.

Wern, J. O. 1980. A study of the macrobenthos of the brackish lakes in Sea Rim State
Park, Texas and contiguous Keith Lake. Unpublished M.S. thesis, Texas A & M Univ.,
College Station, 215 pp.

RCH at: biology@hal.lamar.edu
* * *

REPRODUCTION IN THE WESTERN HOGNOSE SNAKE,
HETERODON NASICUS (SERPENTES: COLUBRIDAE) FROM
THE SOUTHWESTERN PART OF ITS RANGE

Stephen R. Goldberg

Department of Biology, Whittier College
Whittier, California 90608

The western hognose snake, Heterodon nasicus ranges from southern
Canada to San Luis Potosi, Mexico and southeastern Arizona to central
Illinois where it frequents prairies, open woodlands and floodplains of

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THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 3, 2004

rivers; in the extreme western part of its range it occurs in semidesert
habitats (Stebbins 2003). Most of the information on reproduction in
this species was reported by Platt (1969) who studied a Kansas popula¬
tion of H. nasicus. Anecdotal information on reproduction is in: Marr
(1944); Werler (1951); Moore (1953); Wright & Wright (1957); Fitch
(1970); Pendlebury (1976); Tennant (1984); Lowe etal. (1986); Taggart
(1992); Iverson (1995); Degenhardt et al. (1996) and Stebbins (2003).
Ernst & Ernst (2003) summarized information on reproduction in H.
nasicus. Information on the biology of this species is in Walley &
Eckerman (1999). The purpose of this paper is to present the first
reproductive data on H. nasicus from the southwestern part of its range
based on a histological examination of reproductive tissues from museum
specimens. Studying the reproductive cycle in different parts of a
snake’s range allows one to see the extent of geographic variation in
reproduction within a species. Also presented is the first histological
evidence that H. nasicus females initiate yolk deposition (= secondary
vitellogenesis sensu Aldridge 1979) during late summer in follicles that
will be ovulated the following year.

A sample of 37 specimens of H. nasicus (19 females, mean snout- vent
length, SVL = 480.4 ± 71.3 SD, range: 361-613; 18 males, SVL =
324.3 mm + 34.9 SD, range: 290-390 mm) from Arizona, New Mexico
and Mexico was examined from the herpetology collections of Arizona
State University (ASU), the Natural History Museum of Los Angeles
County, Los Angeles (LACM) and the University of Arizona, Tucson
(UAZ). Most snakes (33/37) 89% were from Arizona. Snakes were
collected 1949-1999. Counts were made of enlarged follicles > 8 mm
length or oviductal eggs. The left testis, vas deferens and a portion of
the kidney were removed from males; the left ovary was removed from
females for histological examination (except for females with enlarged
follicles or oviductal eggs which were counted). Tissues were embedded
in paraffin and sectioned at 5 [im . Slides with tissue sections were
stained with Harris’ hematoxylin followed by eosin counterstain. Testes
slides were examined to determine the stage of the male cycle; ovary
slides were examined for the presence of yolk deposition (secondary
yolk deposition sensu Aldridge 1979). Some snakes were road-kills so
not all tissues were available for examination. Number of specimens
histologically examined by reproductive tissue were: testis = 18, vas
deferens = 16, kidney = 18, ovary = 16. Male and female mean
body sizes were compared using an unpaired Mest.

TEXAS J. SCI. 56(3), AUGUST, 2004

269

Table 1 . Monthly distribution of conditions in seasonal testicular cycle of Heterodon nasicus
from examination of museum specimens. Values shown are the numbers of males
exhibiting each of the three conditions.

Month

Regressed

Recrudescence

Spermiogenesis

May

June

July

August

September

October

Material examined.— The following specimens of Heterodon nasicus
were examined: ARIZONA: COCHISE COUNTY, (ASU 22859, LACM
109514, 115794, 145667, UAZ 9365, 24934, 24935, 24937, 24938, 24941,
24942, 35159, 39611, 39612, 39617, 39618, 40146, 41146, 41147, 41152,
43892, 46321, 46322, 46833, 48011, 50017, 51822) GRAHAM COUNTY,
(ASU 7029, 22461) SANTA CRUZ COUNTY, (UAZ 40778, 43756, 43799,
50066). NEW MEXICO: HIDALGO COUNTY, (ASU 31499) LUNA
COUNTY, (LACM 109527). MEXICO: CHIHUAHUA, (UAZ 39198,
39199).

Testicular histology was similar to that of the two colubrid snakes,
Masticophis taeniatus and Pituophis catenifer ( = P. melanoleucus ) as
reported by Goldberg & Parker (1975). In the regressed testes, semi¬
niferous tubules contained spermatogonia and Sertoli cells. In recrudes¬
cence (recovery) there was renewal of spermatogenic cells characterized
by spermatogonial divisions; primary and secondary spermatocytes were
typically present. In spermiogenesis, metamorphosing spermatids and
mature sperm were present. Testes undergoing spermiogenesis were
found August-October (Table 1). Testes from the two spring males (one
from May and one from June) were regressed. The smallest reproduc-
tively active male (spermiogenesis in progress) measured 290 mm SVL
(UAZ 46322). Platt (1969) found motile spermatozoa in cloacal smears
of 3/7 (43%) H. nasicus < 300 mm SVL from Kansas. As was the
case for Kansas (Platt 1969), H. nasicus from the southwestern extreme
of its range undergoes a postnuptial spermatogenesis = aestival sperma¬
togenesis ( sensu Saint Girons 1982) which is completed before winter
with sperm stored over winter in the vas deferens. All vasa deferentia
(n = 16) contained sperm: May (1), August (2), September (6), October
(7). Tubules of all kidney sexual segments, except for the one July male
17/18 (94%), were enlarged and contained secretory granules: May (1),
June (1), August (2), September (6), October (7), a condition that

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THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 3, 2004

Table 2. Monthly distribution of conditions in seasonal ovarian cycle of Heterodon nasicus
from examination of museum specimens. Values shown are the numbers of females
exhibiting each of the four conditions; *squashed oviductal eggs, clutch could not be
counted.

Month

Inactive

Early yolk
deposition

Enlarged follicles
> 12 mm length

Oviductal

eggs

May

June

July

August

September

October

typically coincides with breeding (Saint Girons 1982). According toPlatt
(1969), the principal H. nasicus mating period is in the spring, although
some mating may also occur in autumn.

Females were significantly larger than males (t = 8.4, df = 35, P <
0.0001). One female H. nasicus from Cochise County, Arizona with
five oviductal eggs (UAZ 24941) was collected 28 May. Another,
(UAZ 24938) from Cochise County, with six enlarged follicles (> 8
mm length) was collected 6 June. A third female from Cochise County
collected in July (ASU 22859) contained squashed oviductal eggs that
could not be counted. Females with early yolk deposition (secondary
yolk deposition sensu Aldridge (1979) were found June-September
(Table 2). This yolk deposition was in the form of a small band of
discrete yolk granules. Because the yolk occupied only a limited area
of the follicles it would have been unlikely for yolk deposition to have
been completed during the current reproductive season. However, since
Platt (1969) reported H. nasicus deposits eggs in August (locality not
given), one must consider the possibility that in some females, yolk
deposition might have been completed during the current year. How¬
ever, it appears that in at least some cases H. nasicus females initiate
yolk deposition (vitellogenesis) the summer prior to completing it. For
example (Fig. 1), early yolk deposition is present in UAZ 43892, a
road-kill from 31 July in which the two largest follicles had lengths of
2 mm. It is doubtful that these follicles would have completed yolk
deposition in the current year. These findings agree with Ernst & Ernst
(2003) who reported a complement of small follicles in H. nasicus
females which represent ova to be matured the following year. There
was a report of an August Hypsiglena torquata female with yolk
deposition in Goldberg (2001). Whether starting yolk deposition in the

TEXAS J. SCI. 56(3), AUGUST, 2004

271

Figure 1. Yolk deposition in ovarian follicle of Heterodon nasicus (UAZ 43892) collected
31 July 1980. Bar represents 15 /xm.

summer prior to ovulation is common in North American colubrid
snakes needs to be investigated.

The two clutch sizes reported herein (5, 6) are near the lower end of
the ranges for H. nasicus 4-23 clutch sizes reported by Platt (1969) and
4-25 reported by Stebbins (2003). The smallest reproductively active
female (yolk deposition in progress, UAZ 39611) measured 361 mm
SVL. This was close to the smallest gravid H. nasicus female (SVL =
366 mm) from Kansas (Platt 1969). Eight female H . nasicus from
Harvey County, Kansas deposited egg clutches from 2-23 July (Platt
1969). The presence of one Arizona female H. nasicus (UAZ 24941)
with oviductal eggs on 28 May and a female from Valencia County,
New Mexico that deposited eggs on 12 June (Degenhardt et al. 1996)
may suggest that females from the southern portion of the range produce
eggs earlier in the year than females from the northern part. Small
sample sizes prevent an analysis of geographic variation in clutch sizes,
although Fitch (1985) found no evidence of geographic change in clutch
sizes between northern and southern populations of H. nasicus.

In conclusion, there does not appear to be differences in the timing of
the seasonal testicular cycle of H. nasicus between Kansas and the south-

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THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 3, 2004

western part of its range in that sperm produced in autumn are stored
through winter in the vasa deferentia in both areas. There is a sug¬
gestion that eggs may be produced earlier in the season in the south.
Additional females need to be examined to determine if this occurs. It
appears that some H . nasicus females initiate yolk deposition (vitello¬
genesis) in follicles the summer before eggs are produced.

Acknowledgments

I thank Andrew T. Holycross (Arizona State University), George L.
Bradley (University of Arizona) and David A. Kizirian (Natural History
Museum of Los Angeles County) for permission to examine H. nasicus

Literature Cited

Aldridge, R. D. 1979. Female reproductive cycles of the snakes Arizona elegans and
Crotalus viridis. Herpetologica, 35(3) :256-261 .

Degenhardt, W. G., C. W. Painter & A. H. Price. 1996. Amphibians and reptiles of New
Mexico, University of New Mexico Press, Albuquerque, xix + 431 pp.

Ernst, C. H., & E. M. Ernst. 2003. Snakes of the United States and Canada. Smithsonian
Books, Washington, ix + 668 pp.

Fitch, H. S. 1970. Reproductive cycles of lizards and snakes. Misc. Publ. Mus. Nat.
Hist., Univ. Kansas, 52:1-247.

Fitch, H. S. 1985. Variation in clutch and litter size in New World reptiles. Misc. Publ.
Mus. Nat. Hist., Univ. Kansas, 76:1-76.

Goldberg, S. R. 2001. Reproduction in the night snake, Hypsiglena torquata (Serpentes:

Colubridae), from Arizona. Texas J. Sci., 53(2): 107-1 14.

Goldberg, S. R. & W. S. Parker. 1975. Seasonal testicular histology of the colubrid
snakes, Masticophis taeniatus and Pituophis melanoleucus. Herpetologica,

3 1 (3):3 1 7-322.

I verson, J. B. 1995. Heterodon nasicus (Western Hognose Snake). Reproduction.
Herpetol. Rev., 26(4):206.

Lowe, C. H., C. R. Schwalbe & T. B. Johnson. 1986. The venomous reptiles of Arizona.

Arizona Game & Fish Department, Phoenix, ix + 115 pp.

Marr, J. C. 1944. Notes on amphibians and reptiles from the central United States. Am.
Midi. Nat., 32(2):478-490.

Moore, J. E. 1953. The Hog-nosed snake in Alberta. Herpetologica, 9(4): 173.
Pendlebury, G. B. 1976. The western hognose snake, Heterodon nasicus nasicus, in
Alberta. Can. Field Natur., 90(4) :4 16-422.

Platt, D. R. 1969. Natural history of the hognose snakes Heterodon platyrhinos and
Heterodon nasicus. Univ. Kansas Publ., Mus. Nat. Hist., 18(4):253-420.

Saint Girons, H. 1982. Reproductive cycles of male snakes and their relationships with
climate and female reproductive cycles. Herpetologica, 38( 1 ) :5- 16.

Stebbins, R. C. 2003. A field guide to western reptiles and amphibians, 3rd ed. Houghton
Mifflin Company, Boston, Massachusetts, xiii + 533 pp.

Taggart, T. W. 1992. Observations on Kansas amphibians and reptiles. Kansas Herpetol.
Soc. Newsletter, 88:13-15.

Tennant, A. 1984. The snakes of Texas. Texas Monthly Press, Inc., Austin, 561 pp.
Walley, H. D., & C. M. Eckerman. 1999. Heterodon nasicus Baird and Girard. Western

TEXAS J. SCI. 56(3), AUGUST, 2004

273

hognose snake. Cat. Amer. Amphib. Rept., 698.1-698.10.

Werler, J. E. 1951. Miscellaneous notes on the eggs and young of Texan and Mexican
reptiles. Zoologica, 36(l):37-48.

Wright, A. H. & A. A. Wright. 1957. Handbook of snakes of the United States and
Canada. Vol. I., Comstock Publ. Assoc., Ithaca, New York, xviii -I- 564 pp.

SRG at: sgoldberg@whittier.edu

* * *

ENDOPARASITES OF THE SEQUOYAH SLIMY SALAMANDER,
PLETHODON SEQUOYAH (CAUDATA: PLETHODONTID AE) ,

FROM MCCURTAIN COUNTY, OKLAHOMA

Chris T. McAllister and Charles R. Bursey

Department of Biology, Texas A&M University -Texarkana
Texarkana, Texas 75505 and

Department of Biology, Pennsylvania State University -Shenango Valley Campus
Sharon, Pennsylvania 16146

The Sequoyah slimy salamander, Plethodon sequoyah , is a medium¬
sized plethodontid that is restricted to McCurtain County, Oklahoma
(Conant & Collins 1998) and perhaps adjacent Sevier County, Arkansas
(Trauth et al. 2004). This salamander occurs in upland forests where it
inhabits seeps and springs hiding beneath rocks, clumps of moss, or
under decaying logs. This species, one of several belonging to the P.
glutinosus group 10 complex, was described by Highton (1989) as hav¬
ing a unique Mdh-2 allele that distinguishes it from 15 other species of
the P. glutinosus group. In addition, this evolutionary lineage has also
been recognized by Powell et al. (1998) and Duellman & Sweet (1999),
and most recently was included on a list of standard and common
current scientific names (Collins & Taggart 2002).

Although information is available on parasites of other species within
the P. glutinosus complex (Baker 1987; McAllister et al. 1993; 2002),
nothing, to the authors’ knowledge, has been published on protozoan or
helminth parasites of P. sequoyah. This study provides the first report
of endoparasites from this host.

Twenty-five juvenile and adult salamanders (mean + 1 SD snout- vent
length [SVL] = 46.5 ± 14.3, range 24-74 mm) were collected by hand,
two on 13 September 2002, six on 3 June 2003, and 17 on 15 April
2004 from Beaver’s Bend State Park, McCurtain County, Oklahoma
(33° 7.7’N, 94° 41.9’W, elev. 153.6 m). Specimens were placed in

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THE TEXAS JOURNAL OF SCIENCE- VOL. 56, NO. 3, 2004

damp collecting bags on ice and returned to the laboratory within 24h
for processing. Specimens were killed by prolonged immersion in a
dilute Chloretone® solution. For necropsy, a midventral incision was
made and the entire gastrointestinal tract, liver, gallbladder, spleen and
gonads were examined for helminths. Blood smears were taken from
the exposed heart and stained with DifQuick. Feces from the colon and
rectum were collected and placed in individual vials containing tap water
supplemented with antibiotic (100 I. U./mL penicillin-G 100 pgt mL
streptomycin) and examined directly without sucrose flotation by
microscopy for coccidia. The integument was examined closely for
intradermal mites (Hannemania) . Tapeworms were relaxed in cold tap
water, fixed in 70% ethanol, stained with Semichon’s acetocarmine and
mounted entire with Permount®. Nematodes were placed in a drop of
glycerol on microscopic slides and identifications were made from these
temporary mounts. Flelminth voucher specimens were deposited in the
United States National Parasite Collection (USNPC), Beltsville,
Maryland, USA, and the Harold W. Manter Laboratory of Parasitology,
Lincoln, Nebraska, USA: Cepedietta michiganensis (HWML 45996),
Cylindrotaenia idahoensis (USNPC 94810, 95245), Mesocestoides sp.
(USNPC 94811), Batracholandros magnavulvaris (USNPC 94812,
95246), Cosmocercoides variabilis (USNPC 94813). Host voucher
specimens were deposited in the Arkansas State University Museum of
Zoology (ASUMZ 27250, 27920-27924) and University of Oklahoma
Museum of Natural History (OMNH 39181).

Eighteen of 25 (72%) of the P. sequoyah were infected with one of
five parasite species, including one (4%) with Cepedietta michiganensis
in the small intestine, seven (28%) with Cylindrotaenia idahoensis (mean
intensity 6.3, range 1-19) in the small intestine, two (8%) with Meso¬
cestoides sp. in the mesenteries and peritoneal cavity, three with
Cosmocercoides variabilis (mean intensity 9.7, range 5-17, 13 females,
16 males) in the rectum, and eight (32%) each with a single female of
Batracholandros magnavulvaris in the rectum; six salamanders (24%)
harbored multiple infections. Blood smears were negative for hemato-
zoa, the feces did not contain coccidia, and none of the salamanders
were infested with Hannemania .

The astomatous ciliate, C. michiganensis has been reported previously
from various salamanders and frogs (Joy & Tucker 2001; McAllister &
Bursey 2004), including the Fourche Mountain salamander, P. fourchen-
sis , western slimy salamander, P. albagula, and Rich Mountain sala-

TEXAS J. SCI. 56(3), AUGUST, 2004

275

mander, P. ouachitae from Arkansas (Winter et al. 1986; McAllister et
al. 1993; 2002), and the southern redback salamander, P. serratus from
Oklahoma (McAllister et al. 2002). This study represents the first
report of this protist in P. sequoyah.

The cyclophyllidean tapeworm, C. idahoensis was originally described
from the Coeur d’Alene salamander, P. idahoensis from Idaho (Waitz
& Mehra 1961). Since then, this cestode has been reported in Jordan’s
redcheek salamander, P. jordani from North Carolina (Dyer 1983; Jones
1987), the western redback salamander, P. vehiculum from Oregon
(Panitz 1969), and the Caddo Mountain salamander, P. caddoensis, P.
ouachitae and P. serratus from Arkansas and Oklahoma (McAllister et
al. 2002). This study documents a new host record for the parasite in
P. sequoyah.

The cestode, Mesocestoides sp. is an enigmatic tapeworm whose
complete life cycle is unknown. The initial report in salamanders of the
world was by McAllister et al. (1995) who reported this parasite in eight
of 41 (20%) Ouachita dusky salamanders, Desmognathus brimleyorum
from Arkansas. This study reports a second salamander host for this
tapeworm. This cestode has also been previously reported from various
anurans (McAllister & Conn 1990).

The ascarid nematode, C. variabilis has been commonly reported
from both amphibians and reptiles in the United States and Canada
(summarized by McAllister & Bursey 2004). This parasite (as Oxy-
somatium sp.) has also been previously reported from Oklahoma in
bullfrogs, Rana catesbeiana (Trowbridge & Hefley 1934); however, this
study reports a new host for this roundworm.

The nematode, B . magnavulvaris is a pinworm with a direct life cycle
that exhibits little host specificity. It has been previously reported in P.
caddoensis , P. fourchensis, P. ouachitae , P. serratus and D.
brimleyorum in Arkansas and Oklahoma (Winter et al. 1986; McAllister
et al. 1995; 2002). In addition, this parasite has a wide geographic
range as it has been reported in salamanders of the genera Aneides,
Desmognathus , Eurycea, Leurognathus , Notopthalmus from California,
Illinois, Michigan, New Hampshire, North Carolina, Pennsylvania,
Tennessee, Virginia and West Virginia (see Joy & Tucker 2001 for
summation). Plethodon sequoyah represents a new host for this parasite.

276

THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 3, 2004

In summary, although no new geographic records are documented,
this study provides the first report of endoparasites from P. sequoyah.
Several parasite species reported herein are shared with other Plethodon
sp., and as in previous surveys on salamanders, this limited data
supports Aho’s (1990) suggestion that the parasite community structure
is depauperate and noninteractive.

Acknowledgments

The senior author thanks Joel Johnson (Univ. Oklahoma), Boy Scout
Troop 1, Indian Nations Council, Tulsa, and the Spring 2004 TAMU-T
Herpetology class (especially Zach Ramsey) for assistance in collecting,
and the Oklahoma Department of Wildlife Conservation for Scientific
Collecting Permit Nos. 3172 and 3376. We also thank Drs. Dan
Brooks and Bruce Conn for examining the Mesocestoides sp.

Literature Cited

Aho, J. M. 1990. Helminth communities in amphibians and reptiles: comparative ap¬
proaches to understanding patterns and processes. Pp. 157-195, in Parasite Communities:
Patterns and Processes (G. W. Esch, A. O. Bush, and J. M. Aho, eds), Chapman and
Hall, New York, 304 pp.

Baker, M. R. 1987. Synopsis of the Nematoda parasitic in amphibians and reptiles. Mem.

Univ. Newfoundland Occas. Pap. Biol., 11:1-325.

Collins, J. T. & T. W. Taggart. 2002. Standard common and current scientific names for
North American amphibians, turtles, reptiles & crocodilians. 5th Edition. Center for
North American Herpetology, Lawrence, Kansas, 44 pp.

Conant, R. & J. T. Collins. 1998. A field guide to reptiles and amphibians of eastern and
central North America. 3rd Edition, expanded. Houghton Mifflin, Boston, Massachusetts,

616 pp.

Duellman, W. E. & S. Sweet. 1999. Pp. 31-109, in Patterns of Distribution of Amphibi¬
ans: A Global Perspective (W. E. Duellman, W. E. ed), Johns Hopkins University Press,
Baltimore, viii + 633 pp.

Dyer, W. G. 1983. A comparison of the helminth fauna of two Plethodon jordani popu¬
lations from different altitudes in North Carolina. Proc. Helm. Soc. , Washington 50:257-
260.

Highton, R. 1989. Part 1. Geographic protein variation. Pp. 1-78, in Biochemical Evolu¬
tion in the Slimy Salamanders of the Plethodon glutinosus Complex in the Eastern United
States (R. Highton, G. C. Maha, and L. R. Maxson, eds). Illinois Biol. Monogr., 57:1-
153.

Jones, M. K. 1987. A taxonomic revision of the Nematotaeniidae Liihe, 1910 (Cestoda:

Cyclophyllidea). Syst. Parasitol., 10:165-245.

Joy, J. E. & R. B. Tucker. 2001. Cepedietta michiganensis (Protozoa) and Batracholandros
magnavulvaris (Nematoda) from plethodontid salamanders in West Virginia, U.S.A.
Comp. Parasitol., 68:185-189.

McAllister, C. T. & C. R. Bursey. 2004. Endoparasites of the dark-sided salamander,
Eurycea longicauda melanopleura, and the cave salamander, Eurycea lucifuga (Caudata:
Plethodontidae), from two caves in Arkansas, U.S.A. Comp. Parasitol., 71:61-66.

TEXAS J. SCI. 56(3), AUGUST, 2004

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McAllister, C. T. & D. B. Conn. 1990. Occurrence of Mesocestoides sp. tetrathyridia
(Cestoidea: Cyclophyllidea) in North American anurans (Amphibia). J. Wild. Dis., 540-
543.

McAllister, C. T., S. J. Upton & S. E. Trauth. 1993. Endoparasites of western slimy
salamanders, Plethodon albagula (Caudata: Plethodontidae), from Arkansas. J. Helm.
Soc. Washington, 60:124-126.

McAllister, C. T., C. R. Bursey & S. E. Trauth. 2002. Parasites of four species of
endemic Plethodon from Arkansas and Oklahoma. J. Arkansas Acad. Sci., 56:239-242.

McAllister, C. T., C. R. Bursey, S. J. Upton, S. E. Trauth & D. B. Conn. 1995. Parasites
of Desmognathus brimleyorum (Caudata: Plethodontidae) from the Ouachita Mountains
of Arkansas and Oklahoma. J. Helm. Soc. Washington, 62:150-156.

Panitz, E. 1969. Helminth parasites of salamanders of the genus Plethodon in western
Oregon. Canadian J. Zool., 47:157-158.

Powell, R., J. T. Collins & E. D. Hooper, Jr. 1998. A key to the amphibians and reptiles
of the continental United States and Canada. University Press of Kansas, Lawrence,
Kansas, vi + 131 pp.

Trauth, S. E., H. W. Robison & M. V. Plummer. 2004. The amphibians and reptiles of
Arkansas. University of Arkansas Press, Fayetteville, Arkansas, xv + 421 pp.

Trowbridge, A. H. & H. M. Hefley. 1934. Preliminary studies of the parasite fauna of
Oklahoma anurans. Proc. Oklahoma Acad. Sci., 14:16-19.

Waitz, J. A. & K. N. Mehra. 1961. Baerietta idahoensis n. sp. a nematotaeniid cestode
from the intestine of Plethodon vandykei idahoensis from northern Idaho. J. Parasitol.,
47:806-808.

Winter, D. A., W. M. Zawada & A. A. Johnson. 1986. Comparison of the symbiotic
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Arkansas Acad. Sci., 40:82-85.

CTM at: chris.mcallister@tamut.edu

278

THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 3, 2004

Plan Now for the
108th Annual Meeting of the
Texas Academy of Science

March 3 - 5, 2005
University of Texas-Pan American

Program Chair
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Phone: 512.292.4200
E-mail: dwaitt@wildflower.org

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FAX: 956.381.3657

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2007 - Baylor University

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279

IN RECOGNITION OF THEIR ADDITIONAL SUPPORT OF
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The Texas Academy of Science
CMB 5980
Schreiner University
Kerrville, Texas 78028-5697
E-mail : FStevens@schreiner . edu

THE TEXAS JOURNAL OF SCIENCE

Volume 56, No. 4

November, 2004

CONTENTS

Potential Causes of a Decline in American Beech (Fag us grandifolia Ehrh.)
in Wier Woods, Texas.

By S. Jha, P. A. Harcombe, M. R. Fulton and 1. S. Elsik . 285

Comparative Analysis of Growth and Mortality Among Saplings in
a Dry Oak-Pine Forest in Southeast Texas.

By Jie Lin, Paul A. Harcombe, Mark R. Fulton and Rosine W. Hall . 299

Structural Changes after Prescribed Fire in Woody Plant Communities of
Southeastern Texas.

By Changxiang Liu, Paul A. Harcombe and Robert G. Knox . 319

Growth of Chinese Tallow Tree ( Sapium sebiferum ) and Four Native Trees under
Varying Water Regimes.

By Bradley J. Butterfield, William E. Rogers and Evan Siemann . . . 335

Effects of Temperature and Mulch Depth on Chinese Tallow Tree (Sapium sebiferum )
Seed Germination.

By Candice Donahue, William E. Rogers and Evan Siemann . 347

The Effect of Mycorrhizal Inoculum on the Growth of Five Native Tree Species
and the Invasive Chinese Tallow Tree (Sapium sebiferum).

By Somereet Nijjer, William E. Rogers and Evan Siemann . 357

Characterization of Arthropod Assemblage Supported by the Chinese Tallow Tree
(Sapium sebiferum) in Southeast Texas.

By Maria K. Hartley, Saara DeWalt, William E. Rogers and Evan Siemann . 369

Diel Activity Patterns of the Louisiana Pine Snake (Pituophis ruthveni)
in Eastern Texas.

By Marc J. Ealy, Robert R. Fleet and D. Craig Rudolph . 383

Arboreal Behavior in the Timber Rattlesnake, Crotalus horridus,
in Eastern Texas.

By D. Craig Rudolph, R. R. Schaefer, D. Saenz and R. N. Conner . 395

Nesting Habitat of Eastern Wild Turkeys (Meleagris gallopavo sylvestris)
in East Texas.

By Bobby G. Eichler and R. Montague Whiting, Jr . 405

The Red-Cockaded Woodpecker: Interactions with Fire, Snags, Fungi,

Rat Snakes and Pileated Woodpeckers.

By Richard N. Conner, Daniel Saenz and D. Craig Rudolph . 415

Feeding Habits of Songbirds in East Texas Clearcuts During Winter.

By Donald W. Worthington, R. Montague Whiting, Jr. and James G. Dickson . . . 427

Index to Volume 56 (Subject, Authors & Reviewers) . 441

Recognition of Member Support . 453

Membership Application . 454

Postal Notice . 455

THE TEXAS JOURNAL OF SCIENCE
EDITORIAL STAFF

Managing Editor:

Ned E. Strenth, Angelo State University
Manuscript Editor:

Robert J. Edwards, University of Texas- Pan American
Associate Editors for this Issue:

Paul Harcombe, William Marsh Rice University

Craig Rudolph, U.S. Forest Service

Evan Siemann, William Marsh Rice University

Manuscripts intended for publication in the Journal should be
submitted in TRIPLICATE to:

Dr. Robert J. Edwards
TJS Manuscript Editor
Department of Biology
University of Texas-Pan American
Edinburg, Texas 78541
r edwards@panam . edu

www . texasacademy ofscience . org

AFFILIATED ORGANIZATIONS
American Association for the Advancement of Science,
Texas Council of Elementary Science
Texas Section, American Association of Physics Teachers
Texas Section, Mathematical Association of America
Texas Section, National Association of Geology Teachers
Texas Society of Mammalogists

The 3rd Big Thicket Science Conference, "Biodiversity and Ecology of
the West Gulf Coastal Plain Landscape", was held October 9-11, 2003 in
Beaumont, Texas. The Big Thicket is a biologically rich area within the
West Gulf Coastal Plain where the influences of southeastern swamps,
eastern deciduous forests, central plains, pine savannas and xeric sandhills
meet and intermingle. The region provides habitat for many rare species
and favors unusual combinations of plants and animals. The purpose of the
Big Thicket Science Conference is to highlight the results of recent
ecological research and conservation efforts to understand, manage and
restore the unique biological diversity of the Big Thicket and surrounding
West Gulf Coastal Plain. The event brought together a diverse group of
individuals representing government, academia, conservation organizations,
private industry and local residents.

It took the efforts of many people to produce this document. Numerous
people reviewed the manuscripts included in this volume. We appreciate
their input that greatly improved the quality of the manuscripts and their
willingness to review manuscripts in a short period of time. We thank the
contributing authors for their patience with the editorial process. We thank
the Texas Academy of Science for their support of this project. We are
particularly grateful to Ned Strenth for his assistance as managing editor.
We hope this publication increases our understanding of the biological
resources of this region.

The 4th Big Thicket Science Conference is scheduled for Fall 2007.
Information regarding this event will be forwarded to registered participants
of the 3rd conference. Other interested parties may contact: Chief of
Resources Management, Big Thicket National Preserve, 3785 Milam,
Beaumont, Texas 77701 (phone: 409.839.2689).

Big Thicket Science Conference
Publication Committee

Paul Harcombe, William Marsh Rice University
Maxine Johnston, Big Thicket Association
Wendy Ledbetter, The Nature Conservancy
Ricky Maxey, Texas Parks and Wildlife
Craig Rudolph, U.S. Forest Service
Evan Siemann, William Marsh Rice University

Program Committee

Judy Aronow, Lamar University Center for the Study of the Big Thicket

James Barker, Big Thicket National Preserve

Carroll Cordes, U.S. Geological Survey

Deanna Fusco, Big Thicket National Preserve

Cathy Guivas, Big Thicket National Preserve

Paul Harcombe, William Marsh Rice University

Chuck Hunt, Big Thicket National Preserve

Fulton Jeansonne, Big Thicket National Preserve

Maxine Johnston, Big Thicket Association

Wendy J. Ledbetter, The Nature Conservancy

Ricky Maxey, Texas Parks and Wildlife Department

Kim McMurray, Entergy, Inc.

Jim Neal, U.S. Fish and Wildlife Service
Jeff Pittman, Lamar University
Craig Rudolph. USD A Forest Service
Evan Siemann, William Marsh Rice University

Underwritten by:
Entergy, Inc.

Sponsored By:

Beaumont Convention & Visitors Bureau
Big Thicket Association
ExxonMobil Corporation

Lamar University’s Center for the Study of the Big Thicket
National Park Service (Big Thicket National Preserve)
The Nature Conservancy
Texas Parks & Wildlife Department
USD A Southern Research Station
USGS National Wetlands Research Center
U.S. Fish & Wildlife Service
William Marsh Rice University

TEXAS J. SCI. 56(4):285-298

NOVEMBER, 2004

POTENTIAL CAUSES OF A DECLINE IN AMERICAN BEECH
( FAGUS GRANDIFOLIA EHRH.) IN WIER WOODS, TEXAS

S. Jha, P. A. Harcombe, M. R. Fulton
and I. S. Elsik

Department of Ecology and Evolutionary Biology
Rice University, Houston, Texas 77005

Abstract.— In a mature southern mixed hardwood stand in Hardin County, Texas,
American beech ( Fagus grandifolia) declined in basal area by 38% between 1985 and 2001,
and 59% of the largest trees (>45 cm dbh) died (4.10%/yr). The mortality rate was nearly
triple that of understory trees (4.5-14cm dbh) (1.13%/yr). Mortality increased in 1987
following a hurricane, and remained high for the 15-year duration of the study. Dead trees
were aggregated in space, causing the population to change in distribution from regular to
random. Evidence for pathogen damage was mostly circumstantial. Night-time tempera¬
tures, to which beech is susceptible, have been increasing over the last 20 years. No single
factor (increasing temperatures, moderate hurricane damage, or pathogens) alone appears
sufficient to explain the decline of large American beech trees in this forest over the past 20
years. Instead, a combination of factors seems most likely.

Southern mixed forests contain an unusually high diversity of woody
plant species (Marks & Harcombe 1975). In general, they exhibit a
successional trend towards dominance by beech and magnolia (Gano
1917; Kurz 1944; Glitzenstein et al. 1986), though the mixed species
nature of these southern hardwood forests is hypothesized to result from
complex disturbance regimes (Glitzenstein et al. 1986; Platt & Schwartz
1990). In addition to its shade tolerance and longevity, American beech
may also be resistant to exogenous damage caused by tropical storms
(Batista et al. 1998; Batista & Platt 2003). Consequently, beech-domi¬
nated forests might be expected to be relatively stable. However, a
beech population in southeast Texas showed substantial decline between
1987 and 1999 (Harcombe et al. 2002). In this paper, the decline is
analyzed and several hypotheses are tested to explain it.

One possible explanation could be a hurricane which hit the site in
1986. Within southern mixed hardwood forests, hurricanes can slow the
replacement of shade-intolerant species by shade tolerant species
(Glitzenstein et al. 1986; Cain & Shelton 1995; Arevalo et al. 2000).
Peters & Poulson (1994) suggested that hurricanes may limit beech
dominance in beech forests around the world. However, there is also
contrary evidence; hurricanes did not strongly reduce American beech
growth rates in northern Florida (Batista et al. 1998) or in east Texas
(Bill 1995).

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THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 4, 2004

Another possible explanation involves climate change. Recent model¬
ing research indicates that American beech distribution within the United
States is governed by temperature, precipitation, soil, and elevation-
related variables (Iverson & Prasad 1998). Box et al. (1993) define the
climatic space corresponding to the geographic species range as a
"climate envelope." The envelope for American beech involves, among
other measures, a relatively moist climate and maximum daily tempera¬
tures between 17°C and 29°C. Davis & Zabinski (1992) modeled the
distribution of American beech with respect to temperature and predicted
that if temperature increased, species at their southern range limits,
including American beech, would exhibit immediate declines in seedling
density and an eventual decline of canopy trees after a few decades of
warming. Other studies in North America have also suggested that
increasing summer temperature significantly reduces American Beech
growth (Fritts 1958; Tubbs & Houston 1990, Tardiff et al. 2001).
Finally, a recent dendroecological study in Texas showed high sensitivity
of American beech to temperature and precipitation between the summer
months of May and July (Cook et al. 2001). Particularly in east Texas,
where American beech reaches its southwestern range limit, increasing
summer temperatures may exceed heat tolerance limits of the species,
affecting growth and mortality.

American beech is also vulnerable to sucking insects, decay fungi,
and pathogens (Tubbs & Houston 1990). The most notorious example
is Beech Bark Disease, which has affected American beech trees in the
northeastern United States (Ehrlich 1934; Houston et al. 1979). In the
southern United States, the bark canker fungus Hy poxy Lon atropunctatum
has been documented on American beech trees (Thompson 1963; Pase
2002). Hy poxy Ion first affects the cambium; it is thought to be triggered
by low moisture in the xylem and can take three to four years to kill a
tree (Pase 2002). Aphid infestation can also damage beech; it has
recently been documented in east Texas (Hemmingsen 2002; Siemann
& Rogers 2003).

A variety of abiotic and biotic factors clearly influence American
beech populations. Declines of woody species could also be related to
species population structure and natural population dynamics (reviewed
in Mueller- Dombois 1992). Furthermore, population dynamics may be
strongly influenced by the series of stresses each individual in a popula¬
tion experiences. Manion (1981) classified stresses into two categories:
"predisposing factors," which are long term stresses, and "inciting
factors, " which are short-duration stresses. Pederson (1998) showed that
trees with a negative response to a prior stress were more likely to have

JHA ET AL.

287

a negative response to a subsequent stress. Thus, tree mortality can be
the result of a variety of factors that act over a lifetime, and growth and
mortality may be synchronized in a population that has a history of
stresses.

The hurricane, changing climate conditions, and pathogens could be
acting together or separately, along with stress history or population
structure, to cause the decline of American beech in Wier Woods. In
this paper, these hypotheses are examined by analyzing 22 years of data
on spatial and temporal variation in beech growth, recruitment, and
mortality.

Study Site

The study site is a 4 ha plot in Wier Woods Preserve (The Nature
Conservancy), located about 16 km north of Beaumont, Hardin County
(30° 16’ N, 94° 12’ W), Texas (Figure 1). Wier Woods is located 140
km east of the western range limit of the species (McLeod 1975), just
5 km north of the southern range limit for American beech (Little 1971).
The site is part of the Big Thicket (Marks & Harcombe 1981), a 2500
km2 forested region located 50-100 km inland from the Gulf of Mexico.
The soil is a siliceous, thermic, Susquehanna fine sandy loam (Deshotels
1978). Average annual temperature is 20.4°C, with a long growing
season (approx. 240 days) from March to November (Harcombe et al.
2002). Species composition in the Wier Woods is typical of southern
mesic forests (Quarterman & Keever 1962; Blair & Brunett 1976;
Glitzenstein, et al. 1986). The important species in Wier Woods include
loblolly pine (Pinus taeda), water oak ( Quercus nigra), American beech
(Fagus grandifolia) , southern magnolia (Magnolia grandiflora) , and
white oak (Quercus alba) (Harcombe et. al. 1998). Glitzenstein et al.
(1986) found that disturbance at Wier Woods may accelerate early
successional stands of pine and oak towards beech and magnolia domi¬
nance and also re-initiate new regeneration of pine and oak in areas
currently dominated by beech and magnolia. Harcombe et al. (2002)
noted the rapid decline in basal area of beech, in spite of increases in
most other species and an overall increase in stand basal area.

On June 26, 1986, Hurricane Bonnie, with winds estimated at 120
km/hr, passed over the site (Doyle & Girod 1997; NOAA 1986).

Methods

Data for this research are from a permanent sample plot of approxi¬
mately 4 ha. An irregular polygon was divided into 101 contiguous 20
by 20 m cells, and stems with DBH > 4.5 cm were tagged and
mapped; species identity and DBH was measured for each stem. All

288

THE TEXAS JOURNAL OF SCIENCE— VOL. 56, NO. 4, 2004

Fig. 1. American beech distribution in southeastern U.S.A. (Little 1971).

tagged trees were measured in May or June of 1980, 1982, 1985, 1987,
1989, 1992, 1995, 1998, and 2001. All stems that had reached 4.5 cm
DBH since the last measurement (ingrowth) were tagged and mapped.

Trees with missing or anomalous DBH values were assigned an
interpolated value. Trees missed in earlier surveys were assigned DBH
values by back projection, based on calculated mean growth rates for the
appropriate time period, species, size, and class (Bill 1995). All of the
interpolated values were used in calculations of basal area and density,
but not in calculations of growth rates, even though they had only a
small effect on growth values. Data were analyzed using SAS (SAS
Institute) or Microsoft Excel (ver. MS2000). Average annual growth
rates were calculated by dividing change in DBH by the number of years
between measurements.

Mortality surveys were conducted annually, and percent mortality was
calculated as the number of individuals found dead in a single year
divided by the number of individuals in the living population in the
previous year. The possible existence of a temporal pattern in mortality
(as opposed to a random fluctuation) was evaluated by comparing two
models of large beech mortality using the Akaike Information Criteriron
or AIC (Burnham & Anderson 2002). The AIC incorporates both the
likelihood of the data given in the model, and the number of free
parameters in the model; the model with the lowest AIC is considered
to be the best supported by the data. The first model assumed a constant
probability of mortality, with the average mortality rate as the one free
parameter. The second model approximated mortality by a step

JHA ET AL.

289

function, with one probability before and one probability after the step.
For this model there were three free parameters: the first and second
mortality probabilities and the time of the step between the two.

Mortality as a function of DBH was also predicted with logistic re¬
gression using the Weibull distribution (Antle & Wain 1988). Models
were fitted for the intervals six years before Hurricane Bonnie (198 1 -
1986), the year immediately after the hurricane (1987), six years after
the hurricane (1987-92), and the 14 years after the hurricane (1987-
2001).

The Clark- Evans Nearest Neighbor Test (Clark & Evans 1954) was
used to test for aggregation of the American beech population. Because
distributions at any time are highly influenced by the prior population
distribution, a randomization test was also performed to determine
whether mortality was aggregated given the initial spatial distribution.
The test calculates the mean nearest neighbor distances for dead and live
trees where the null hypothesis takes the initial spatial distribution of the
population as a given. The null distribution is created by shuffling the
identity of living and dead trees 1000 times.

Meteorological data (NOAA 2002) were obtained for Liberty, Texas,
56 km west of the study site. This station provided the longest temporal
record within a reasonable distance. Less-extensive records from the
Beaumont Research Station, 16 km from the study site, were also
examined; they indicated similar weather patterns. Mean temperature
of the warmest month was calculated by averaging the daily minimum
and the daily maximum for the summer months and then averaging the
daily averages to get monthly means. The century average for the
August mean temperature was also calculated. To calculate the mean
temperature of the coldest month, this same procedure was repeated for
the month of January. Night-time temperature of the coldest month was
approximated by averaging the daily minimum temperatures in the
month of January. An annual moisture index (annual precipitation/
potential evapotranspiration; Box et al. 1993) was calculated. Potential
evapotranspiration for Wier Woods was obtained from Caird (1996).
Average precipitation of the driest month was calculated by summing
daily precipitation per month, calculating the century average for each
month, and then choosing the driest month.

For the age distributions of American Beech individuals at Wier
Woods, data were used from 136 tree cores extracted from a random
sample of the tree population as reported by Glitzenstein (1984;
Glitzenstein et al. 1986).

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THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 4, 2004

160

4.5-14cm

□ individuals in 1980
m individuals in 2001

■

15-29cm 30-45cm > 45cm

DBH class

Fig. 2. Number of individuals in 1980 and 2001 by DBH class.

Results

Population trends.— The original population of American beech trees
tagged in 1980 consisted of 153 individuals > 4.5 cm DBH. Basal area
of beech was 4.0 m2/ha, 11.5% of stand basal area. By 2001, basal
area of beech had declined to 2.7 m2/ha in spite of an overall increase
in stand basal area from 34.7 to 36.4 m2/ha. The decline was strongly
concentrated in the largest trees; the number of individuals > 30 cm
dropped and the number of smaller individuals rose between 1980 and
2001 (Fig. 2). The > 45 DBH class experienced mortality at a rate of
4.10%/year, more than double the rate for the smaller size classes
(Table 1). Mortality of largest trees was consistently higher than that of
the whole population across the 20-year study period (Fig. 3). The
step- function mortality model was significantly better in predicting large
tree mortality than was the model assuming a constant probability of
mortality over time (AIC of 257 vs. 267); the best step function was the
one in which the increase occurred in 1986.

Average tree growth rates were variable. Dying large trees did not
show significantly lower growth before mortality than surviving large
trees (FU66 = .50, />=0.48).

Hurricane Beech mortality was high in 1987, the survey after the
storm. Nevertheless, this was not the highest yearly mortality rate

JHA ET AL.

291

Table 1. Percent mortality of American beech by size class six years before Hurricane
Bonnie (1981-1986), one year after the hurricane (1987), six years after the hurricane
(1987-92), the average across the study period (1981-2001), and the maximum annual

rate.

Size Class
(cm DBH)

Six Years
Before

One Year
After

Six Years
After

Average

Highest

4.5 - 14

0.90

0.00

0.97

1.13

4.08 (1996)

15 - 30

0.00

1.85

1.55

10.00 (1992)

30 - 45

0.52

6.90

1.67

1.70

14.81 (1995)

>45cm

1.16

7.80

5.92

4.10

13.89 (1990)

total

0.77

3.52

2.50

2.03

5.11 (1990)

□ % mortality total population

years

Fig. 3. Percent mortality of total beech population (dark bars) and large individuals of beech
(light bars).

across the long-term study (Fig. 3, Table 1). Rather, Wier Woods lost
most of its large trees gradually between 1987 and 2001. Mortality in
the storm interval itself was not significantly different from the six years
before the storm (x2 test; df— 1, P=. 282); however, mortality was
significantly greater after the storm than before for both the six-yr
interval (x2 test, df= 1, P< .001) and the entire post-hurricane interval
(x2 test, df— 1 , P— .031). Logistic regressions of mortality versus DBH
show the same pattern, i.e., that there was a significantly higher
probability of mortality after the storm interval than before (for both the
six-year and 15-year intervals) but not between the pre-storm interval
and the storm interval itself (Fig. 4).

Climate.— After 1972, minimum temperature in August for Liberty,
Texas rose steadily through 2001. In fact, 21 of last 23 summers ex¬
ceeded the century average for minimum summer temperature, while
precipitation showed no trends (Fig. 5). Wier Woods was above the

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THE TEXAS JOURNAL OF SCIENCE— VOL. 56, NO. 4, 2004

•e

<4—

>»

•O

0 20 40 60 80

Diameter at breast height (cm)

Fig. 4. Logistic regression curves of probability of mortality of American beech as a
function of DBH for (a) six years before Hurricane Bonnie (1981-1986) (b) the census
year including the hurricane (1987), (c) the six years after the hurricane (1987-92), and
(d) the 15 years after the hurricane (1987-2001). Dashed lines represent 95% confidence
intervals.

climate envelope of American beech for mean temperature of the warm¬
est month (34° vs 29 °C) but did not go below the bottom of the enve¬
lope for mean minimum temperature in the coldest month (15° vs 9°C).
The annual moisture index (precipitation/potential evapotranspiration) ,
was slightly below the minimum threshold (1.0 vs 1.1). Mean precipi¬
tation of the driest month was above the minimum threshold (88 vs 40
mm).

Pathogens /pests .—Dying trees had thin canopies and exhibited sub¬
stantial leaf yellowing. Otherwise, none of the dying beech trees
exhibited physical characteristics that might suggest death was caused by
pathogens or parasites.

Spatial aggregation analysis showed that in 1980 living American
beech trees of all sizes were uniformly distributed (R= 1.11, P< .01)

JHA ET AL.

293

Year

Fig. 5. Meteorological data from Liberty, Texas, (a) Minimum August temperatures.
Dashed lines represent average minima for 1906-1980 (21.9°C) and for 1981-2002
(23.2°C). (b) Summer (May, June, July) precipitation. The solid line represents average
summer precipitation for 1905-2002.

according to the Clark Evans nearest neighbor test. Large individuals
were also uniformly distributed (R— 1.27, P< .01). Large trees dying
between 1980 and 2001 were significantly aggregated (R= .65, P< .01),
causing large living trees in 2001 to be randomly distributed. The
randomization test confirmed that mortality was significantly aggregated
(P< .05), even considering the initial distribution of the population.

Synchronous death. —The age distribution (Fig. 6) shows that beech
trees have been germinating steadily since 1850, except for peaks in

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THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 4, 2004

1820-1870 and 1910-1950. Minima in ring widths in the 1920s and
1950s suggest that the population experienced two important periods of
marked environmental change, the pine logging of 1917 and the drought
of 1950 (Glitzenstein, et al. 1986). The drought of the 1950s was
indeed the longest and worst in the state’s climate history registering
"severe" on the Palmer Drought Severity Index (NOAA 2003).

Discussion

Beech mortality was clearly not randomly distributed in time or space,
nor was the population even-aged, and so the decline is neither a conse¬
quence of a random fluctuation in large-tree mortality nor a result of
synchronous death of an even-aged population; there was a significant
decline beginning in 1987 in an all-aged population. To explain this
decline, predisposing stress, pest/pathogen, and hurricane disturbance
are considered independently, and then a combination of these causes is
proposed.

Stress. — Stress due to drought is one of the most common factors that
predispose populations to respond negatively to environmental stresses
in the future (Pederson 1998). However, the 1950s drought occurred
many years ago and so it is hard to imagine it had a major effect (but
see Pederson 1998). A more immediate stress is the summer tempera¬
tures that are outside the climate envelope of beech, as defined by Box
et al. (1993), recalling the high sensitivity of beech ring widths to
August temperature (Cook et al. 2001). Large trees may be especially
prone to temperature-related stress because of their greater exposure to
sunlight and higher respiration.

Further support for climate stress is provided by recent range limit
studies for American beech. For example, Iverson & Prasad (1998)
predicted current distribution of American beech to be north of its actual
distribution range, and Davis & Zabinski (1992) predicted that the
American beech population would shift north if temperatures increased.
The proximity of Wier Woods to the southwestern range limit of beech
(Fig. 1) is relevant in this context since the influence of changing
temperature would logically be expected to appear here first.

Pathogens /pests. —Two influences, aphid infestation (Siemann &
Rogers 2003) and Hypoxylon (Pase 2002), have been documented on
American beech in east Texas. However, neither aphids nor patches of
their ‘honey dew’ secretions, were noted to be particularly abundant in
Wier Woods during annual mortality surveys. Also, aphid feeding has
minimal impact on large mature trees, causing its greatest damage and

295

JHA ET AL.

Approximate Decade of Germination

Fig. 6. The age distribution of a random sample of the beech population at Wier Woods

based on ring counts from increment cores gathered by Glitzenstein (1986).

dieback in small trees less than 3 meters tall (Hemmingsen 2002) .

Hypoxylon- infected water oaks are common, but Hypoxylon fungal
cankers were observed on only a single beech tree in Wier Woods in a
special inspection conducted in May 2003. Furthermore, patterns in
growth rates at Wier Woods do not support the hypothesis that a fungal
pathogen is causing beech decline. At Wier Woods, growth rates of
dying large trees were not lower than those for living large trees, as
might have been expected (see Houston 1979). However, it should be
noted that the sample size for growth rates was small, and growth rate
trends may be unclear given a small sample size and the inherently low
growth rates of large, old trees.

Although there is little direct evidence for an effect of Hypoxylon , the
aggregated mortality of large beech trees is consistent with the influence
of a pathogen (but see below). A pathogen might also explain the
extended duration of high mortality at Wier Woods, since pathogens
may take months or years to affect their host (Hepting 1971), rather than
causing mortality in one short time period. Given the high susceptibility
of American beech to pathogens, the wide variety of pathogens known
to affect beech, and the difficulty in documenting pathogen influences,
this possible cause cannot be completely ruled out.

Hurricane .—In a mesic forest in northern Florida, after a hurricane
more severe than Hurricane Bonnie, Batista et al. (1998) found that
large American beech trees experienced moderate direct hurricane
mortality (8.2%) and low overall post-hurricane mortality (Batista &
Platt 2003). Assuming that a more intense storm would cause greater
immediate damage to large American beech trees (Batista et al. 1998,
Batista & Platt 2003), the lower immediate mortality and higher post-

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THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 4, 2004

hurricane mortality in Wier Woods suggests that Hurricane Bonnie was
not intense enough to account for the decline of the beech population.
Furthermore, although the hurricane could have resulted in delayed
mortality (cf., Putz & Brokaw 1989), mortality has remained high for
more than 15 years after the hurricane, which suggests that other factors
are influencing population mortality.

Synthesis. — Tree population declines occasionally may be the result
of a single environmental factor, but they most often have multiple
causes (Manion 1981). Some of these are predisposing factors, occur¬
ring months or even years, before tree mortality, and others are inciting
factors precipitating an episode of mortality (Houston 1987). The
hurricane could have been such an inciting factor. By damaging trees,
it might have triggered an increase in mortality (Putz & Brokaw 1989)
in a population already weakened by a predisposing factor such as the
consistently increasing summer temperatures in the 1980s and 1990s.
Pathogens often appear on host species after periods of climate stress,
and trees weakened by climate stresses (Houston 1987) or hurricane
injury (Putz & Brokaw 1989) can be especially susceptible to attacks of
insects or fungi. Hurricane damage to the crowns of large beech trees
could also increase heat loading on remaining nearby trees and could
therefore explain the spatial aggregation of mortality.

Thus stress due to high summer temperatures, in conjunction with
hurricane disturbance and possible pathogen influence, provides the most
consistent hypothesis to explain the observed decline in American beech
at Wier Woods. Further empirical observation of this beech population,
as well as surveys of other beech populations in southeast Texas, will be
required to fully evaluate this hypothesis.

Acknowledgments

We thank Saara DeWalt and Jie Lin for their advice on statistics and
SAS; the Wier family and the Nature Conservancy for permission to
work in Wier Woods; and Peter Marks (Cornell University) David
Appel (Texas A&M University) and Elgene Box (University of Georgia)
who shared their thoughts and research results with us.

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PAH at: harcomb@rice.edu

TEXAS J. SCI. 56(4): 299-3 18

NOVEMBER, 2004

COMPARATIVE ANALYSIS OF GROWTH AND MORTALITY
AMONG SAPLINGS IN A DRY OAK-PINE FOREST
IN SOUTHEAST TEXAS

Jie Lin, Paul A. Harcombe, Mark R. Fulton1
and Rosine W. Hall2

Department of Ecology and Evolutionary Biology
Rice University, Houston, Texas 77251-1892
Present address:

department of Biology, Bemidji State University
1500 Birchmont Dr. NE, Bemidji, Minnesota 56601
department of Biology, Auburn University at Montgomery
7300 University Drive, Montgomery Alabama 36117

Abstract.— The role of shade tolerance in the dynamics of a sandy upland pine-oak forest
in Big Thicket National Preserve, southeast Texas was investigated. Using a forest dynamics
modeling framework, radial growth of saplings as a function of light availability and
mortality as a function of recent growth history for species with a range of shade tolerance
levels was investigated. In low light, shade-tolerant species grew faster than shade-intolerant
species. However, in high light, shade-intolerant species did not grow faster than shade-
tolerant species possibly because some of them are adapted for drought resistance. They did
not survive better, either, perhaps because of recent increases in canopy shading. Mesic,
shade-tolerant species had better performance at the dry site than at the mesic site, possibly
because of a difference in the competitive environment of the two sites. An implication of
invasion and higher growth and survival of the mesic species is that these species may have
been limited to a larger extent by fire than by site conditions on this site in the past.

Broad patterns in species dominance across the landscape are well
known for the southeastern United States (Christensen 1988; Ware et al.
1993), and these are consistent with general understanding of physio¬
logical tolerances of the major tree species. In southeast Texas,
interspecific differences in response to light are consistent with trends in
species dominance at a mesic site (Lin et al 2001; 2002), and thereby
help provide mechanistic underpinning for observed species dominance
on mesic sites. At a wet site, light was important in helping to explain
species dominance, but only if response to flooding was considered, as
well (Hall 1993; Hall & Harcombe 1998; 2001; Lin et al. 2004). In the
study reported here, analysis of the light response to a dry site is
extended, partly to further investigate the effects of site differences on
light responses, and partly also to determine whether differences in light
response among species help explain changes in species dominance.

The approach is based on the general understanding that light, soil
moisture and nutrients are important factors that determine species

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THE TEXAS JOURNAL OF SCIENCE— VOL. 56(4), 2004

composition of many terrestrial plant communities (e.g. Huston & Smith
1987; Smith & Huston 1989; Pacala et al. 1994; Knox et al. 1995; Sipe
& Bazzaz 1995; Grubb et al. 1996; Catvosky & Bazzaz 2000). Mortali¬
ty-growth-light relationships based on the forest dynamics model,
SORTIE (Pacala et al. 1993; 1994; 1996; Kobe et al. 1995) are used.
The model assumes resource competition among coexisting species, as
do most forest dynamics models (e.g. Botkin et al. 1972; Shugart 1984;
Smith & Huston 1989; Pacala et al. 1996). Through repeated iterations
of the model, light competition results in shifting dominance from shade-
intolerant species to shade- tolerant species over the course of stand
development. Extending SORTIE by incorporating soil moisture into
the mortality-growth model, Caspersen & Kobe (2001) found that
species ranks in mortality-growth relationship shifted substantially across
soil moisture gradient, resulting in shifting dominance.

Although competition for soil moisture provides a possible process-
level explanation for the broad pattern of species segregation across the
landscape in southeast Texas (Marks & Harcombe 1981; Harcornbe et
al. 1993) and across the southeastern United States (Christensen 1988;
Ware et al. 1993), fire also plays a role (Harcombe et al. 1993; 1998).
Under the fire scenario, sites with longleaf pine ( Pinus palustris ), a
species highly tolerant to fire, would not support mature hardwood
forests. One way to investigate the question of the relative importance
of soil moisture and fire is to compare growth-mortality relationships of
species under different moisture regimes. In essence, this is asking
whether consistency can be found between process (growth/mortality)
and pattern, and tie it to a mechanism (competition for light and/or
mois-ture). If growth and mortality for species present at different sites
are lower at the dry site, the inference that soil controls vegetation
pattern cannot be ruled out. If, on the other hand, growth and mortality
are higher at the dry site under the current fire suppression scenario,
then fire may have been the major limiting factor at the dry site in the
past.

In this study, light competition in a mixed pine-oak stand in the
Turkey Creek Unit of the Big Thicket National Preserve, southeast
Texas was investigated. In addition, growth and mortality of species
common to both this dry site and a nearby mesic site were compared.
Compared with the mesic site, the dry site is characterized by coarser
soils and lower soil moisture availability (Caird 1996). Widespread
presence of charcoal on stumps and the prevalence of longleaf pine

LIN ET AL.

301

indicates that the dry site probably burned relatively frequently
(Harcombe et al. 1993). Under the current fire suppression scenario,
the site is being invaded by mesic species (Harcombe et al. 1998). The
invasion of mesic species suggests that they may have been limited by
fire in the past, and not by low soil moisture. The following questions
are addressed: Do differences in mortality-growth-light relationship
among species within and between sites explain differences in dominance
between the dry site and the mesic site? Can species responses to site
conditions explain differences in species composition or must historical
disturbances (e.g., fire) be invoked?

Study Sites and Species

The dry study site is located on a low, sandy ridge in the Turkey
Creek Unit of the Big Thicket National Preserve about 10 km southeast
of Warren, Tyler County, Texas (30°35’N, 94°24’W). The climate of
the area is humid subtropical with an annual rainfall around 1475 mm.
The soil is a sandy loam of Landman series, loamy, siliceous thermic
Grossarenic Paleudalf (Caird 1996). Light measurements obtained from
hemispherical photos taken at plot centers (100 plots in total) indicated
a light range in the understory from 1.7% full sun to 33.5% full sun
with a mean of 12.8%.

The vegetation is dominated by oaks and pines. Ranked in decreasing
order of relative abundance, post oak ( Quercus stellata Wang.), southern
red oak (Quercus falcata Michx.), black hickory (Cary a texana Buckl.),
longleaf pine (Pinus palustris Mill.), loblolly pine (Pinus Taeda L.) and
shortleaf pine (Pinus echinata Mill.) form a relatively open canopy
15-20 m tall. Basal area increased from 21m2/ha in 1982 to 28 m2/ha
by 1999. Red maple (Acer rub rum L.) and sweetgum (Liquidambar
styraciflua L.) are minor canopy components. The understory is a
moderately dense mixture of tree saplings and shrubs; flowering dog¬
wood (Comus florida L.), yaupon (Ilex vomitoria Ait.) are abundant.
Saplings of mesic species, such as Southern magnolia (Magnolia grandi-
flora L.) and American holly (Ilex opaca Ait.) have become more abun¬
dant since 1980 (Harcombe et al. 1998). American holly and flowering
dogwood are very shade-tolerant; sweetgum and most dry-site species
are shade- intolerant. The above shade tolerance categories are based on
conventional wisdom regarding shade tolerance as summarized by Burns
& Honkala (1990). These shade tolerance classifications are based
largely on field observations regarding the relative abundance of differ¬
ent species in the forest understory.

302

THE TEXAS JOURNAL OF SCIENCE-VOL. 56(4), 2004

Table 1. Latin names, common names, name codes and shade tolerance of major species.
Species are arranged in ascending order of shade tolerance according to Burns & Honkala
(1990).

Latin Name

Common

Name

Species

Code

Shade

Tolerance

Site

Affiliation

Quercus stellata

Post oak

QUST

Intolerant

Dry

Cary a texana

Black hickory

CATE

Intolerant

Dry

Pinus palustris

Longleaf pine

PIPA

Intolerant

Dry

Pinus echinata

Shortleaf pine

PIEC

Intolerant

Dry

Pinus Taeda

Loblolly pine

PITA

Intolerant

Mesic, dry

Liquidambar styraciflua

Sweetgum

LIST

Intolerant

Mesic, dry

Quercus falcata

Southern red oak

QUFA

Intermediate

Dry

Acer rubrum

Red maple

ACRU

Tolerant

Mesic, dry

Magnolia grandiflora

Southern magnolia

MAGR

Tolerant

Mesic, dry

Ilex opaca

American holly

ILOP

Very tolerant

Mesic dry

Comus florida

Flowering dogwood

COFL

Very tolerant

Mesic, dry

The dry site was logged in 1930 but the stand is not strongly
even- aged (Harcombe et al. 1993; Kaiser 1995); apparently many old
hardwoods and older pines were left in the site. Exactly how long ago
fire occurred on this site is unknown. The presence of charcoal on
stumps implies relatively frequent fire prior to 1930 and relatively
infrequently after that until 1974. Fire has been absent since 1974
(Kaiser 1995; P. Harcombe, personal communication).

A nearby mesic site was chosen for comparison. The mesic site is
located in Hardin County, Texas (30°16’N, 94°12’W) approximately 14
km away from the dry site. Species composition of this site represents
many typical mesic sites throughout the Coastal Plain area of the south¬
eastern U.S. (Marks & Harcombe 1981). The site is dominated by
loblolly pine ( Pinus taeda L.), water oak ( Quercus nigra L.), white oak
(Quercus alba L.), American beech ( Fagus grandifolia Ehrh.) and
southern magnolia ( Magnolia grandiflora L.). Red maple (Acer rubrum
L.), blackgum (Nyssa sylvatica Marsh.) and sweetgum (Liquidambar
styraciflua L.) are abundant as small to medium stems but are infrequent
as large trees. Important understory trees include American holly (Ilex
opaca Ait.) and flowering dogwood (Comus florida L.). Basal area has
varied between 33.7 m2/ha (after hurricane) and 35.1 m2/ha over the last
20 years. More detailed description can be found in Glizenstein et al.
(1986) and Lin et al. (2001; 2002). See Table 1 for shade tolerances
and affiliations of species with sites.

LIN ET AL.

303

Data Collection and Analyses

Sapling growth. — The dry study site is 4 ha divided into 100 con¬
tiguous tree plots. Each plot is 20m by 20m. Tree surveys were
performed in 1980, 1982, 1985, 1989, 1994, 1997 and 2000. During
tree surveys, stems with a Diameter at Breath Height (DBH) > 2 cm
are measured with a diameter tape. A subset of 16 plots was chosen
randomly for annual measurement of saplings (height > 140 cm and
DBH <4.5 cm), in which DBH of all saplings was measured to the
nearest 0. 1 cm from 1980-2000. All trees and saplings are tagged with
an identification number. For each sapling (height > 140 cm and DBH
<4.5 cm), annual radial growth rate over three years was calculated as
the difference in radius between year 1999 and year 1996 divided by 3.
The average over 3 years was used to reduce measurement variation.
Calculations of growth were made for all species with more than 15
individuals in the sample.

As approximations of high-light growth and low-light growth, top
quartile growth rate (TQGR) and bottom quartile growth rate (BQGR)
were calculated. Approximations were chosen because it was not
possible to model mortality-growth-light relationships owing to small
sample sizes and/or insufficient range of light conditions, TQGR is a
reasonable approximation of high- light growth because saplings that have
high growth rates are unlikely to be growing in low light. Comparison
of TQGR and the actual high-light growth in the mesic site where both
measures are available showed a good agreement between the two (data
not shown). It is important to note that bottom quartile growth rate is
only a rough approximation of low-light growth because low growth
could result from many reasons other than low light.

Top quartile growth rate was computed as follows: First, the radial
growth rate over the first 3 years after the sapling first entered the
survey was calculated. After calculating growth rates of all first-year
saplings, growth rates were sorted in descending order. Then saplings
with growth rates in the top 25% were chosed and their growth rates
were averaged. To see whether TQGR of first-year sapling obtained
this way might underestimate maximum growth, it was compared with
TQGR for all saplings present in one period (1996-1999); it did not
(results not shown) . The bottom quartile growth rates were obtained by
taking the bottom 25% growth rates and computing the average.

Light measurement.— A subset of live saplings was selected from the

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THE TEXAS JOURNAL OF SCIENCE— VOL. 56(4), 2004

database for light measurements. In keeping with the protocols of
previous studies, the goal was to find at least 50 saplings per species for
light measurement. The final sample size ranged from 45 to 59 saplings
per species. The six species are: red maple, sweetgum, loblolly pine,
post oak, Southern magnolia and American holly. Saplings were
selected in a stratified random fashion by plot to obtain a broad range
of light conditions. Fish-eye photographs were taken at the top of each
sapling (following Rich 1989; Pacala et al. 1994) in mid summer (late
June to mid July), 1999. To increase contrast, all photos were taken
early in the morning before sunrise and late in the afternoon after sunset
when skylight is evenly distributed. Moreover, all photos were taken on
Kodak TMAX ASA 400 (black and white) film and the film was under¬
exposed by 1 f-stop to further enhance contrast. The images were
scanned, digitized and analyzed using CANOPY (Rich 1989). Thres¬
hold values were set individually to minimize the “halo effects”
(Anderson 1964). The global site factor (GSF) was estimated from each
photo. GSF is an estimation of the fraction of total radiation (both
diffuse and direct) a sapling experienced during the growing season.
The GSF value was converted to percent of full sun by multiplying GSF
by 100. Since no major canopy disturbances occurred during the 1996-
1999 period, the light level captured in 1999 was considered to be a
reasonable representation of average light environment over the three-
year period at a given location.

Sapling mortality .—In addition to periodic measurement, each sapling
was checked annually to see whether it was dead or alive. Survival time
was calculated as the length of time a sapling was followed during the
course of the study. If a sapling died, then its survival time would be
the difference between the year of death and the year it entered the
study. If a sapling was alive at the end of the study (Year 1999), its
survival time was the difference between the ending year and the year
it entered the study. Saplings that were alive at the end of the study
were flagged as right censored (Cox & Oakes 1984; Lee 1992). All
saplings (dead or alive) that had been recorded since the beginning of
the long-term study (Year 1980) were included. To model mortality as
a function of recent growth, pre-mortality growth rate was calculated for
dead saplings as the difference in radius over the last 3 years prior to
death divided by 3.

Growth-light analysis.— The goal of this analysis is to model growth
response from light availability using a Michaelis-Menten function, as

LIN ET AL.

305

in previous studies (cf. Pacala et al. 1994; Wright et al. 1998). How¬
ever, because of sampling limitations, the asymptote parameter was
replaced by TQGR, which is treated as a constant instead of a para¬
meter, because of inadequate range of conditions and small sample sizes
for some species. The one-parameter model takes the following form:

a/S + L

(1)

Where yu. is the mean growth response given light availability; a is the
TQGR; S is the slope at low light; L is the light availability (% of full
sun).

The maximum likelihood methods to estimate parameter S was used.
The final likelihood function is:

f=l ^27iC[aL/(a/S + L)}'

- exp(-

[Gi

aLKa/S + L)]1 (2)

2 C[aL/(a/S + L)]‘

where Gj is the radial growth rate of sapling i (3-year average); C, D
are two parameters that account for heteroscedasticity.

Confidence intervals of S were obtained by bootstrapping. Both
model fitting and bootstrapping were done using Splus 6.0 on Unix
(Mathsoft, Inc. 2000). A more detailed description of the maximum
likelihood estimation method can be found in Lin et al. (2002).

Mortality risk (annual death rate) as a function of growth.— Survival
analysis was used to model mortality risk as a function of growth. The
likelihood function for censored and non-censored saplings is (Lee
1992):

n*e

i = 1

n~r -Ati

Y\e

i = 1

(3)

where r is the number of saplings that died during the study and n-r is
the number of saplings that are right-censored, f and are lifetimes of
a non-censored and right-censored sapling i, respectively; X is the
parameter of mortality risk (annual mortality risk).

A negative exponential function was used to estimate X from predictor
variables

A = e-0°-P'Xl-0iXlx0

(4)

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THE TEXAS JOURNAL OF SCIENCE-VOL. 56(4), 2004

where Xj is the radial growth rate (mm/yr); X2 is the initial size (radius
in mm). The parameters to be estimated are the fts. 6 is the error term.
Estimates of parameters Bi and ft2 were found by maximizing the
likelihood function (3).

Maximum likelihood estimation of annual death rate— To further
explore how mortality might be different among species with different
shade tolerance, annual death rate was also compared.

The maximum likelihood estimator of annual death rate is (Lee 1992):

(5)

2 =

ZD rj-, yf—~\N-D

Ti+y t,

;=1 Z— (,= 1

Where D is the number of deaths during the time interval

The 95% confidence interval of X is:

~ 2 x 1.96

(6)

Results

Growth response to light and interspecific tradeoff. —Growth in¬
creased with light for all species (Figure 1). Except for sweetgum,
which showed higher growth than red maple, the pattern of low-light
growth was consistent with the expectation that shade-tolerant species
grow faster in low light than shade-intolerant species (Figure 1). The
low-light growth index, slope at low light, was highest for American
holly, followed by southern magnolia (Table 2). Two shade-intolerant
species, loblolly pine and post oak, ranked low in slope (Table 2). The
correspondence between low-light growth and shade tolerance ranks was
further supported by the comparison of bottom quartile growth rates
among species (Figure 2a): Shade-tolerant species ranked higher than
most shade- intolerant species in bottom quartile growth rates, though
bottom quartile growth rate of sweetgum and loblolly pine were higher
than expected based on standard shade tolerance ranks.

In contrast, for high-light growth, the order of TQGR did not cor¬
respond to shade tolerance expectation: First, shade- intolerant post oak
and loblolly pine showed low TQGR; second, shade-tolerant southern
magnolia and American holly grew more rapidly than expected (Figure
1, Table 2). Top quartile growth rates of xeric dominants (e.g., post

LIN ET AL.

307

Percent of full sun (%)

Fig. 1. Fitted growth-light regression curves for different species using equation (1). The
horizontal axis represents percent of full sun (log scale); the vertical axis represents
annual radial growth.

Table 2. Top quartile growth rates (TQGR, a in equation 2) and estimated slope at low light
(S in equation 2) with 95% confidence intervals (Cl). N is the sample size. NA stands
for not available.

Species

Shade

tolerance

TQGR

Cl of
TQGR

Cl of S

Post oak

intolerant

0.905

0.736-1.074

0.026

0.014-0.046

Black hickory

intolerant

0.718

0.641-0.795

Loblolly pine

Intolerant

1.720

1.643-1.798

0.058

0.033-0.099

Sweetgum

Intolerant

2.006

1.912-2.099

0.654

0.357-1.100

Southern red oak

Intolerant

1.263

1.155-1.370

Red maple

Tolerant

1.728

1.599-1.857

0.347

0.232-0.530

Southern magnolia

Tolerant

2.363

2.205-2.516

0.755

0.545-1.123

American holly

Very tolerant

1.847

0.901-1.282

2.911

1.650-5.144

Flowering dogwood

Very tolerant

1.944

1.831-2.057

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THE TEXAS JOURNAL OF SCIENCE— VOL. 56(4), 2004

Bottom quartile growth rates of first year saplings

(N=25)(N=33)(N=25) (N=23) (N=1 6) (N=63) (N=78)(N=31 )(N=121 )

Top Quartile growth rate of first year saplings

I LOP COFL MAGR ACRU QUFA LIST CATE QU ST PITA
(N=25) ( N=33) (N=25) (N=23XN= 1 6) ( N=63) ( N=78) ( N=3 1 ) (N= 1 21 )

Fig. 2. Bottom quartile growth rates for different species (a) and top quartile growth rates
for different species (b). Values not sharing the same letter are significantly different
(ANOVA followed by Tukey’s multiple comparison adjustment, P < 0.05). N is the
number of saplings. Species are arranged in descending order of shade tolerance from
left to right. See Table 1 for key to species codes.

oak, black hickory, southern red oak) were significantly lower (P <
0.05; ANOVA followed by Tukey’s multiple comparison adjustment)
than mesic invaders (e.g., American holly, Southern magnolia, sweet-
gum). Even within the six mesic species, top quartile growth rates did
not conform to expectation: shade-tolerant southern magnolia grew
significantly faster than shade- intolerant sweetgum and loblolly pine
(Figure 2b).

LIN ET AL.

309

Mortality risk as a function of growth.— Mortality risk as a function
of growth was used to characterize shade tolerance in previous studies
(e.g., Kobe et al. 1995; Lin et al. 2001). In this study, the low number
of dead saplings of American holly, southern magnolia and red maple
made survival analysis on these species unreliable (e.g., there was only
one dead American holly sapling and two dead southern magnolia
saplings found in the long-term study data base). Thus, at this site, the
only shade-tolerant species included in survival analysis was flowering
dogwood. In contrast to results of a previous study performed at the
mesic site (Lin et al. 2001), both growth and size were significant
predictors of mortality risk in the dry site. Overall, mortality risk
decreased as growth increased and decreased with increasing size (Table
3). The mortality-growth relationship was not consistent with the
expectation that shade-intolerant species have higher mortality risk at
zero growth and steeper slope than shade- tolerant species (Table 3).

Annual death rare.— Interpretation of the above mortality-growth
responses in terms of shade tolerance expectation was limited by the fact
that only one shade-tolerant species (dogwood) was involved in the
analysis. Therefore, annual death rates among species were also
compared (Figure 3). Mesic species such as American holly, southern
magnolia, red maple exhibited extremely low annual death rate (Figure
3), which is consistent with the previous finding that they have become
more abundant and species typical of dry sites have experienced
dramatic decline (Harcombe et al. 1998). Death rates of dry site
dominants (longleaf pine, post oak, southern red oak) were consistently
higher than mesic site species.

Cross-site comparisons Growth-light curves of southern magnolia
and American holly were significantly higher at the dry site than at the
mesic site over the light range (Figure 4a and b): For red maple,
growth rates were significantly higher only above 60% full sun (Figure
4c). For sweetgum, there was no significant difference between sites
(confidence interval overlapped, not shown) (Figure 4d). Annual death
rates were significantly higher at the mesic site than at the dry site for
all species common to the two sites except flowering dogwood (Figure
5).

Discussion

Growth, mortality and tolerance.— Results show that growth responses
to low light are roughly consistent with one of the expectations regarding
shade tolerance: in low light, shade- tolerant species grow faster than

Table 3. Parameter estimates of the mortality-growth model (equation 4) with 95% confidence intervals (Cl) for different
species. N is the total number of saplings (both dead and live); fis are parameters in equation 4. X is the mortality risk at
zero growth at size class 0.5 mm.

310

THE TEXAS JOURNAL OF SCIENCE- VOL. 56(4), 2004

tj-

Tfr

— *

— 1

TI¬

CG*

<4-

cg"

t}"

<4-

cdf

<4-

a s

>— 1

•n

O s

— H

•n

cg"

1—1

r"~

— <

r~<

ampl

size

1563

441

133

1573

264

178

291

■8 1
« s

Ji3

x: 53
w o

■©

H-H

>— 1

i— ■*

Species

Post oak

Black hickor

Longleaf pin

Shortleaf pin

Loblolly pin<

Sweetgum

Flowering

Dogwood

LIN ET AL.

311

Annual death rate by species

Species

Fig. 3. Annual death rates for different species. Calculation is based on equations 5 and 6.

shade- intolerant species, even on dry sites. However, growth responses
to high light do not correspond to the expected pattern. Instead, two
shade- intolerant species, post oak and loblolly pine, have lower high¬
light growth than expected. Why loblolly pine showed lower high-light
growth than expected remains an interesting question for further investi¬
gation. The low growth of post oak can possibly be explained by
drought tolerance. The inherent conflict between carbon uptake and
water loss of plant has been widely documented and intensively studied
(e.g., Field & Mooney 1986; Huston & Smith 1987). Adapted to soil
water deficiency, drought- tolerant species are reported to develop traits
that minimize water loss but limit growth rates (Delucia et al. 1988;
Kozlowski et al. 1991; Barton & Teeri 1993). Indeed, the three xeric
dominants (post oak, black hickory and southern red oak) in this study
ranked the lowest in both top quartile growth rates and bottom quartile
growth rates (Figure 2) indicating slow growth of drought-tolerant
species (Chapin 1991).

With respect to mortality, the positive association of initial size and
survivorship has also been reported in other studies (e.g. , Clark & Clark
1992; Condit et al. 1995; Sheil & May 1996; Kobe 1999). Compared
with the mesic site (Lin et al. 2001), where a significant effect of size
was not detected, saplings at the dry site span a wider size range, so the
significant effect of size on mortality in this study may be attributable to

312

THE TEXAS JOURNAL OF SCIENCE-VOL. 56(4), 2004

Southern magnolia (Magnolia grandiflora)

American Holly (Ilex opaca)

-• — Mesicsite
•»••• Dry site

(b)

E °

-C

^ 2
o

.2 i
"O 1

. 4 . i . $ . *

a :

Red maple (Acer rubrum)

— \ — l — i — l

0 20

40 60 80 100

Light (% full sun)

Sweetgum (Liquidambar styraciflua)

20 40 60 80

Light (% of full sun)

20 40 60 80

Light (% full sun)

Fig. 4.
light:

Cross-site comparison of fitted radial growth (with 95% confidence interval) vs.
(a) Southern magnolia; (b) American holly; (c) Red maple; (d) Sweetgum.

relatively large size variation (cf. Kobe 1999). In addition, the decline
of mortality with size may be an indication that larger saplings with
more extensive root systems suffer less drought- induced mortality on dry
sites, as suggested by Caspersen & Kobe (2001).

The higher death rate for xeric species than most mesic species
(Figure 3) can possibly be explained in terms of stand dynamics and
change in light environment over the last 20 years. Stem density
increased about 15% from the early 1980s to the 1990s, and most of the
increase in total stem density was caused by increased density of under¬
story dominants, such as yaupon ( Ilex vomitoria ), southern magnolia and
American holly (Kaiser 1995). A direct consequence of an increase in
density of under story species is reduced light penetration to the under¬
story, which would cause the high death rates of shade-intolerant xeric
dominants.

LIN ET AL.

313

Annual death rate comparison

0.08

0.07

0.06
(D

2 0.05

■g 0.04

"CD

| 0.03
<

0.02
0.01
0.00

ILOP MAGR COFL ACRU LIST

Species

Fig. 5. Cross-site comparison of annual death rates. Values not sharing the same letter are
significantly different between the two sites.

As an exception to the pattern of low death rate of shade-tolerant
species, flowering dogwood had a higher death rate than even shade-in¬
tolerant species. This high mortality is consistent with a declining trend
of this species over its range, which is associated with the exotic fungus,
anthracnose ( Discula destructiva) in the Great Smoky Mountains, but not
elsewhere (Schrope 2001). It was noted that fire suppression, which
results in thicker canopy and increased moisture, help the fungus to
thrive (Schrope 2001).

Cross-site comparison and implications for stand dynamics. — Previous
studies have shown that the combined effect of soil moisture and light
on plant performance (growth and survivorship) may largely depend on
the balance between the improvement allowed by one environmental
factor (e.g. , light) and the reduction imposed by deterioration in another
factor (e.g., soil moisture) (Berko witz et al. 1995; Holmgren et al.
1997). At drier sites, if the negative effects of soil moisture deficiency
on plant performance do not outweigh the positive effects of more light
penetration resulting from the more open canopy, then better perfor¬
mance at drier sites would be expected. In fact, many studies have

314

THE TEXAS JOURNAL OF SCIENCE— VOL. 56(4), 2004

reported such “facilitative” effects at drier sites (Parker & Muller 1982;
Barton 1993; Bel sky et al. 1993; Berko witz et al. 1995; Kobe & Coates
1997). In an experiment testing the effects of community composition
on growth and survival of tree seedlings, Berkowitz et al. (1995) noted
that in sites that were physically unfavorable, surrounding vegetation had
few negative effects (competition) on seedling growth. In the case of
sugar maple in their study, surrounding vegetation actually facilitated
growth of sugar maple seedlings. So growth performance was not only
influenced by site suitability, but depended on surrounding vegetation,
as well. This conclusion may provide an explanation for what was
observed. For mesic species (magnolia, American holly and red maple)
in this study, saplings at the dry site may benefit from less competition
for soil resources from slow-growing neighboring vegetation, and
thereby maintain a favorable growth and survival status, even though
there is more total available water at the mesic site than at the dry site
(Caird 1996). The exception, sweetgum, failed to exhibit higher growth
at the dry site possibly because it is less dr ought- tolerant than others
(Marks & Harcombe 1981) and therefore suffered more drought- induced
growth reduction.

The better performance of shade-tolerant mesic species at the dry site
is not consistent with the idea that there is trade-off between shade
tolerance and drought tolerance (e.g., Smith & Huston 1989). Instead,
these species appeared to be both shade- tolerant (i.e. , grow faster and/or
survive better in shade than shade-intolerant species) and drought-
tolerant (i.e. , better performance at dry site than at mesic site). It may
be, however, that differences in drought tolerance only appear in years
of more extreme drought or after saplings get large enough to be
exposed to the drying effect of full sun. Alternatively, Caspersen et al.
(1999) argued that whether species conform to a trade-off between shade
tolerance and drought tolerance may depend on the relative importance
of growth and survival in determining the species ability to tolerate
limiting resources. If the ability to survive in the shade is achieved by
allocation to defense and storage (Kitaj ima 1994; Kobe 1997), then
tolerance to shade may also confer tolerance to other limiting resources,
including soil moisture.

Pacala et al. (1996) argued that light competition can produce
successional patterns in forest communities because of different light
requirements of competing species. In a dry forest, light competition

LIN ET AL.

315

has its apparent signature in growth and mortality of saplings, although
the correspondence between shade tolerance expectation and sapling
performance is weaker than it is at moister sites. The better growth
performance of shade-tolerant invaders in low light than shade-intolerant
dominants, and the correspondence between the decline of shade-
intolerant dominants and canopy closure clearly suggest that this forest
is undergoing successional changes driven by light competition as
suggested by Harcombe et al. (1998); i.e., mesic species do not seem to
be limited by low soil moisture in this forest. Instead, they grow faster
and survive better than at the moister site. While light competition may
be a major driving force of dynamics in this forest, the fact that the light
responses of some species (such as flowering dogwood and sweetgum)
do not conform to the expected pattern of light competition points to the
inadequacies of the SORTIE model. In fact, aside from shade tolerance,
tradeoffs involved in drought tolerance, herbivore tolerance and fire
tolerance may be of importance to explain the observed deviations.

Returning to the question regarding the extent to which the effects of
site conditions and/or fire contribute to stand composition and dynamics,
the data showed that saplings of mesic species have better performance
at the dry site than at the mesic site in terms of both growth and
survivorship. Thus, mesic species do not seem to be limited by site
conditions under the current fire exclusion scenario. An important
implication is that mesic species may have been limited to a larger extent
by fire than by site conditions in the past (Harcombe et al. 1998), and
that the effect of site conditionson vegetation pattern may be as much
indirect via its effect on fire as it is direct via its effect on differential
growth and mortality among species.

Acknowledgments

We thank National Park Service for permission to carry out this study
in Turkey Creek unit. We thank all people participated in collecting the
long-term data set of this forest, especial thanks go to Sandi Elsik who
also manages the data set. Lisa Sweeney helped taking hemispherical
photos in the fields. Cherri Higgins scanned the photos. Scott Baggett
and Evan Siemann provided helpful suggestions on statistical analysis.
Funding for this study was provided by NSF grants to Paul Harcombe
(DEB-9726467) and Mark Fulton (DEB-9816493) and a Wray-Todd
Fellowship to Jie Lin. We thank Kyle Harms and an anonymous re¬
viewer for their comments that improve the manuscript.

316

THE TEXAS JOURNAL OF SCIENCE— VOL. 56(4), 2004

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JL at: jlin@mdanderson.org

TEXAS J. SCI. 56(4):3 19-334

NOVEMBER, 2004

STRUCTURAL CHANGES AFTER PRESCRIBED FIRE
IN WOODY PLANT COMMUNITIES OF
SOUTHEASTERN TEXAS

Changxiang Liu, Paul A. Harcombe and
Robert G. Knox

1527 Weiskopf Loop, Round Rock, Texas 78664,

Department of Ecology & Evolutionary Biology
Rice University, Houston, Texas 77251 and
Biospheric Sciences Branch, Code 923
NASA ’ s Goddard Space Flight Center
Greenbelt, Maryland 20771

Abstract. — A field experiment was conducted to study fire effects on woody plants in
vegetation representing a gradient from dry to mesic types in southeastern Texas. There was
little effect of fire on small sapling density or shrub cover, partly because post-fire recruit¬
ment of saplings by resprouting and germination was rapid. Fire caused declines in large
saplings and small trees in most types, and in large trees in the drier vegetation types. That
is, this study showed that fire effects varied according to vegetation type and stem size class;
the effects were most pronounced for dry types and small trees. The effect of fire on stem
density was lower in the mesic types probably because of differences in moisture, fuel
characteristics, and species response.

Upland communities in the southeastern United States were mostly
dominated by longleaf pine ( Firms palustris Mill.) in presettlement times
(Wahlenberg 1946; Quarterman & Keever 1962; Harcombe et al. 1993;
Ware et al. 1993; Schwartz 1994). Fire was the primary operational
force in maintaining this vegetation pattern (Christensen 1988;
Harcombe et al. 1993; Ware et al. 1993; Schwartz 1994). Logging,
landscape fragmentation and fire suppression contributed to the decline
of longleaf pine communities and expansion of other non-pyric com¬
munities. Prescribed fire has now been reintroduced in preserve lands
across the region, and it is of interest to determine how this will affect
the existing pattern which is a result of varying stand histories and
varying site conditions. The interest derives from the observation that
the response of vegetation may vary in different parts of the landscape
(Christensen 1981; 1988; Romme & Knight 1981; Renkin & Despain
1992; Lertzman & Fall 1998; Breininger et al. 2002).

Some types of vegetation may change substantially if fire is applied
because fires are hot or species are particularly susceptible. Other types
may change little because of low fire intensity caused by specific

320

THE TEXAS JOURNAL OF SCIENCE-VOL. 56(4), 2004

attributes related to vegetation type, including fuel bed characteristics,
soil moisture, and low susceptibility of species. While some of these
factors will have countervailing effects, the general hypothesis is that
mesic vegetation types will show less change than xeric types, primarily
because of denser canopies, less-flammable hardwood litter, and higher
soil moisture content (Marks & Harcombe 1981; Streng & Harcombe
1982; Liu et al. 1997). Higher available soil moisture (related to soil
texture; Harcombe & Marks 1981) favors hardwood species which
produce less-flammable foliage. This, in turn, results in tightly-packed
fuel beds in which lower oxygen availability and higher moisture content
cause fires to be cooler. Also, a site with higher available moisture can
support a denser tree canopy, which can reduce the density of shrubs or
ground-layer species capable of producing flammable fine fuels. Under
these circumstances, even though the species on mesic sites may be
more fire-sensitive, fires are cooler, so the mesic species persist.

Support was found for the hypothesis in a previous report on variation
in species compositional change as a function of vegetation type (Liu et
al. 1997). Although the differences were modest, vegetation types
characteristic of dry sites in the Big Thicket of southeast Texas showed
more compositional change than vegetation types characteristic of mesic
sites. This followup study focuses on changes in structural attributes of
the vegetation (shrub cover, density of saplings and trees). This
provides additional information on the magnitude of the differential
response, and it does so using simple, direct metrics (stem density), as
opposed to the more abstract metric of compositional change (trajectories
in ordination space).

Spatial heterogeneity of the landscape, fire, and vegetation complicate
a study of fire effects; unpredictable change in weather during prescrib¬
ing burning is an additional complicating factor. It is often impractical
to design a completely balanced and controlled experiment. To deal
with these challenges, a field experimental protocol was created with
three components. The first involved sampling more than one vegetation
type in the same burn unit (block); this ensured that the vegetation types
would be burned on the same day under similar weather conditions,
thereby minimizing sources of variation related to weather effects on
fire behavior. The second was to focus on before-after comparisons.
This eliminates spatial variation that would be present in simple com¬
parisons of treatments (burned) and controls (unburned) (Hoshmand
1994). The third was to use control plots for temporal control because

LIU, HARCOMBE AND KNOX

321

the current vegetation is undergoing successional change. Therefore
burned and control blocks may change in different directions if fire does
have effects, or maintain the same trajectory if fire does not have any
effects.

Study Area and Methods

The study area is located in the Big Thicket region of southeast
Texas, an area of about 60 by 60 km between the Trinity and the
Neches Rivers. The southern boundary is about 40 km inland from the
Gulf of Mexico. The area is fairly flat coastal plain that gradually
becomes rolling towards the north. Elevation ranges from a few meters
in the south to about 150 m above sea level in the north (USGS quadran¬
gle sheets, 7.5 minute topographical series, provisional edition, 1984).
From south to north, the Beaumont, Montgomery, Bentley, and Willis
Pleistocene geological formations underlie the area. Soils in uplands and
sandhills are excessively drained, poor in nutrients, and sandy. Soils of
lower slopes, swamps, bottomlands, and floodplains are of loamy or
clayey texture.

The area is warm and humid with a long growing season. Annual
rainfall is 144 cm at Port Arthur, Texas (46-year average) in the
southeast and 125 cm at Livingston (56-year average) in the northwest
(1993 National Climatic Data Center data). Rainfall is evenly distri¬
buted through the year. Annual average temperature is 19.5 °C (30-year
average at Port Arthur).

The vegetation of the Big Thicket is quite similar to that of the rest
of the Coastal Plain of the southeastern United States (Marks &
Harcombe 1981; Christensen 1988; Harcombe et al. 1993) in terms of
community types represented, composition within the major types, and
stand physiognomy. In the Big Thicket, eleven vegetation types have
been recognized and described based on physiography, physiognomy,
and species composition (Marks & Harcombe 1981). Of the eleven
types, seven were considered to be potentially affected by fire and
therefore were sampled in this study. Roughly in the order in which
they appear on a topographic-moisture gradient from dry to wet, they
are as follows: sandhill pine forest (SH), upland pine forest (UP),
upperslope pine-oak forest (US), midslope oak-pine forest (MS), lower-
slope hardwood pine forest (LS), wetland pine savanna (WS), and
wetland shrub baygall thicket (BG). Dominant species in these vegeta¬
tion types are listed in Table 1. Floodplain and flatland types were not

322

THE TEXAS JOURNAL OF SCIENCE-VOL. 56(4), 2004

Table 1. Dominant species in the vegetation types under study.

Vegetation Type

Dominant Species*

Sandhill Pine-Oak

Quercus incana Bartr., Q. stellata Wang, Pinus taeda
L.

Upland Pine

P. palustris Mill., P. taeda, Q. incana

Upperslope Pine-Oak

P. echinata Mill., Q. falcata Michx. , P. palustris, P.
taeda, Q. marilandica Muenchh. Ilex vomitoria Ait.

Midslope Oak-Pine

P. taeda, Q. falcata, P. echinata, Q. alba L.

Lowerslope Pine-Hardwood

Magnolia grandiflora L., Fag us grandifolia Ehrh., P.
taeda, Q. alba, Q. nigra L.

Wetland Pine Savanna

P. palustris, P. taeda, Nyssa sylvatica Marsh., Liquid-
ambar styraciflua L. , Q. falcata, Magnolia virginana L.

Wetland Shrub Baygall Thicket

Q. laurifolia Michx., Nyssa sylvatica, M. virginiana,
Acer rubrum L., Cyrilla racemiflora L., Ilex coriacea
(Pursh) Chapm.

* Nomenclature follows Correll and Johnston (1979).

included because fire does not play an important role in these types.
Data for the LS and BG types were not included in this paper because
attempts to burn the plots of these two types were unsuccessful.

Potential study sites were chosen in the Big Sandy Creek (BS), Lance
Rosier (LR), and Turkey Creek (TC) units of the Big Thicket National
Preserve (BTNP) and in the Roy E. Larsen Sandy lands Sanctuary (RL)
of The Nature Conservancy after a general field reconnaissance. The
following criteria were used in study site selection: (1) presence of
more than one vegetation type in a fire management unit; (2) absence of
obvious recent logging or major natural disturbance; (3) site accessibility
and the possibility of constructing fire breaks; and (4) burning schedules
established by preserve managers.

Within a study site, plots were established in each vegetation type
along a 150 m transect which traversed a uniform area of that type.
Within that vegetation type, four to five 10 by 10 m2 plots were set up
in a burn block along one transect and a corresponding four or five plots
were set up in a control block on a separate transect. Newly constructed
firebreaks separated the burn and control blocks. Plots were located at
random distances along each transect within a treatment (burn or
control) block in each vegetation type. The following observations were
made in each plot:

LIU, HARCOMBE AND KNOX

323

(1) Trees. Stems > 5 cm DBH (large trees) and were measured for
DBH, identified by species, and tagged. Stems 2-5 cm DBH (small
trees) were counted in three categories (2-3 cm, 3-4 cm and 4-5 cm)
by species. Stems were considered alive if they had living tissues
above breast height.

(2) Saplings. Large (DBH < 2 cm but taller than 1.4 m; shrub species
were included in this category) and small (between 0.5 m and 1.4
m in height, tree species only) stems were counted in a 2 by 10 m
strip centered on the central line in each plot parallel with the
transect.

(3) Seedlings ( < 50 cm in height, tree species only) were tallied in a
1 by 10 m strip within the sapling plot by species. Densities of
seedlings and small saplings were combined in analysis.

(4) Shrubs. For clumps of these characteristically multi-stemmed
woody species < 1.4 m tall, cover was measured along an intercept
line with a length of 10 m (in RL) or 20 m (in BTNP) in each plot
parallel with the transect if 1.4 m tall). Larger shrub stems (height
> 1.4 m) were tallied with the large sapling class. When two plots
were so close that the shrub cover measurement would overlap with
that of another plot, the central line was extended accordingly in the
opposite direction along the transect to avoid measurement overlap.

(5) Fuels: fine fuel (1-hour fuel) was collected in a 50 by 50 cm
quadrat at one of the four corners outside the plot and sorted into
duff, needles, leaves, twigs, cones, barks, and live materials.
Sorted samples were dried at 70 °C for 72 hours and weighed. Fuel
depth was measured at 1 m, 3 m, 5 m, 7 m, and 10 m along a 10-m
central line.

(6) Fire temperature: fire-sensitive tablets (Tempil of Big Three
Industries, Inc., New Jersey, USA) were placed in the center of
each plot to obtain a fire temperature estimate. The tablets were
wrapped in aluminum foil and placed 20 cm above ground. Tablets
had following discrete melting points: 52 °C, 101°C, 153°C,204°C,
262°C, 305 °C, 343°C, 399°C, 454°C, 500°C, and 545°C.

For statistical analysis, a nested-factorial analysis was used to
compare fire effects within types by differencing (i.e. , by comparing the
magnitude of change in the burn plots with the magnitude of change in
the controls). About two hundred plots representing 10 sites and five
vegetation types were used in this comparison (Table 2). For burn plots

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THE TEXAS JOURNAL OF SCIENCE— VOL. 56(4), 2004

Table 2. Study plots selected for within-type and cross-type comparisons.

Unit

Site

Vegetation Type

Total

Big Sandy

RC3

Big Sandy

06 3

Big Sandy

15 3

Lance Rosier

Turkey Creek

IS3

Turkey Creek

36 3

Roy Larsen

BF3

Roy Larsen

Total

222

1 Vegetation type: WS— wetland pine savanna; SH— sandhill; UP— upland pine; US— upper-
slope; MS— midslope

2 Treatment: B— Burn; C— Control

3 Sites used for cross-type comparison

at two sites, there was a delay of >2 yr between measurement and
burning, and so preburn values were adjusted to account for the succes-
sional change that would have taken place (based on measured changes
in control plots). Changes in the control plots were generally small for
large saplings and trees, but there were large fluctuations in small
individuals (seedlings and saplings) and in fuel components from year
to year. Because differencing increases variances of adjusted changes
the small individuals were not as useful in addressing fire effects.

The before-after fire comparisons within types involved more than
one site for each type; 4-5 plots were nested within each study site. In
the statistical model, site and plot were treated as factors. Because there
was no replication across sites within burn blocks, the error term was
not retrievable. The following model was used:

Yj = mean + site + plot (site) + time + plot (site) x time
Where Yj — response variable (dependent);

LIU, HARCOMBE AND KNOX

325

mean — overall mean response;

site — site effect;

time — before vs. after;

plot (site) — plot effect nested within site;

plot (site) x time — interaction between time and site;

Here the main focus is the time effect, i.e. is there a significant
difference between post-fire and pre-fire measurements? Because plots
were chosen randomly, effects of plot(site) and plot(site) x time were
treated as random. Because of the unbalanced experimental design
(there are sets of four plots instead of five plots at some sites), a nested-
factorial analysis was preferred to a repeated measurement analysis (SAS
Institute; 1992a; 1992b). The two analyses produce identical results.

To test whether fire had different effects on different vegetation types,
the sites that had more than one vegetation type and were burned on a
single day were chosen. Six sites and four types were appropriate for
such an analysis (Table 2). The four vegetation types that could be
compared were sandhill, upland pine, upperslope, and midslope. Suc-
cessional change unrelated to fire was adjusted for using changes in
control plots as described above for the within- types comparison. How¬
ever, pre-fire differences still existed for the burn plots of different
vegetation types after the adjustment, and so these differences were
adjusted for, as well. The reasoning was that post- fire change measured
in absolute terms might not reflect the fire effects but a combination of
pre-fire difference and fire effect. For instance, a reduction of 50 out
of 100 small trees in an upland pine type by fire is not the same as a
loss of 50 of 500 small trees in a midslope type at the same site. The
former would have a 50% reduction compared to only 10% in the latter.
To overcome this problem, percentage change was calculated with re¬
spect to pre-fire measurement for each site. Thus, the differences in
magnitude of change between types reflected differential effects of fire
on the types. The GLM procedure (SAS Institute 1992a; 1992b) was
used with vegetation type as the only independent variable. Basal area,
shrub cover, density of large saplings, and density of seedling and small
saplings departed somewhat from a normal distribution so a logarithmic

326

THE TEXAS JOURNAL OF SCIENCE— VOL. 56(4), 2004

transformation to the base e was applied after adding one to every
measurement. All transformed data appeared approximately normally
distributed.

Because the response variables were from the same plots and were
possibly correlated, testing the hypotheses for each variable involves
multiple comparisons. Therefore, the error rates (type I error) were
adjusted according to the Dunn-Sidak method (Day & Quinn 1989).
Significant levels were determined by the adjusted error rate according
to Dunn-Sidak method (k = 8). P< =0.0064 (overall error rate of 0.05)
was considered highly significant (**); P< =0.0131 (overall error rate
of 0.10) was considered significant (*); P> 0.0131 (overall error rate
more than 0.10) was not significant (ns) (Figure 1).

Results

Fire reduced fine fuel load in three of the five types, but not in
midslope or savanna (Figure 1). Absence of significant effects in the
midslope type was probably a result of cool and patchy fires (see
below). In the savanna, grasses and forbs recovered quickly after fire
and replaced much of the fuel consumed by fire. Fire reduced fuel
depth (fine fuel only) significantly in all types, though the magnitude of
reduction appeared greater in sandhill and upland pine (Figure 1).
Because heavy needle drop was quite common after hot fires when the
canopy was scorched, fuel consumption in the sandhill and upland types
was probably greater than the data indicated.

Shrub cover was reduced significantly by fire only in the savanna;
other types showed no significant differences between pre- and post- fire
measurements. The rate of post-fire recovery of shrubs by resprouting
was sufficient to return shrub cover to values near pre-fire values,
except in the savanna type, which typically has a sparse understory.
The seedling-small sapling class also showed no significant differences
between pre-fire and post-fire densities, probably because of rapid
resprouting.

Large saplings decreased significantly in density in all types except
midslope after fire. The magnitude of the response was highest in upland
pine and lowest in sandhill. The large saplings consisted mostly of
post- fire survivors; few hardwood species can resprout rapidly and grow
to large sapling sizes (0-1 cm DBH) in one or two years.

LIU, HARCOMBE AND KNOX

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328

THE TEXAS JOURNAL OF SCIENCE-VOL. 56(4), 2004

Small tree density was significantly reduced in all types except
savanna (Figure 2). Since it takes several years for saplings or seedlings
to grow to small tree size, the change can be attributed exclusively to the
direct impact of fire. Large tree density declined significantly in the
sandhill and upland types (Figure 2). Although tree density declined,
the largest trees had high survival, so tree basal area was not signifi¬
cantly affected by the prescription fires.

To compare changes among the types within burn, six blocks were
selected (Table 2) because each of these blocks was burned on a single
day, so the vegetation types being compared were burned under the
same conditions. Since the post-fire values for fuel load, seedling, and
saplings were a combination of fire-related death and recovery after fire
rather than direct fire impact (as described above), the small tree and
large tree strata were emphasized in this cross-type or between-type
comparison. One block (BS10— MS and LS types) was excluded because
the attempt to burn this unit failed.

For four of the six blocks, percentage changes in small tree densities
due to fire differed significantly between the types ( P < 0.005; Figure
3); two of the four also showed significant differences for percent
change in large tree density, as well. The significant differences all
involved comparisons between sandhill or upland pine and other types.
The two blocks (BS15 and BSRC) which showed no significant differ¬
ences in any of the test variables involved comparison between upper-
slope and midslope. The results for all six blocks suggest that fire
affected two dry types (sandhill and upland pine) more strongly than it
did other types.

The greater impact of fire on sandhill and upland pine corresponded
to higher fire intensity. For example, the temperature readings from
upland plots at BS06 were all 152°C to 399°C., whereas fire tablets
melted only in two of the ten upperslope plots (152°C and 204°C). The
differences in fire intensity among types in other sites were similar to
BS06.

In the upperslope - midslope comparisons (BS15 and BSRC), the lack
of significant differences in fire response could be a consequence of cool
fires in both. At BSRC, temperatures ranged from < 52 °C to 253 °C;
At BS15, the fire only partially burned the upperslope plots, and missed
three of the five midslope plots completely.

LIU, HARCOMBE AND KNOX

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Discussion

The effects described here on structural characteristics of stands
(reduced fuel load, reduced sapling and small-tree density, low mortality
of large trees) are consistent with previous finding based on species
composition change (Liu et al. 1997) that the vegetation types in Big
Thicket studied were only moderately sensitive to the prescription fires.
Field observations suggested that an important contributor to this modest
sensitivity was rapid response of small hardwoods by regenerating and
sprouting, a finding corroborated by many other studies (e.g. , Abraham-
son 1984a; 1984b; Westman & O deary 1986; Malanson & Trabaud
1987; Waldrop et al. 1992).

This study focused on short-term effects of prescribed fire. How this
might translate into long-term impact will depend on how the species
respond to repeated fires, whether repeated fire causes a shift in species
composition, and how long the short-term impacts last relative to the
frequency of prescribed burning. In the slope types, fire effects may
disappear in a few years because few large stems are killed by fire. In
the upland types, changes will persist for many years because many
small trees or even large trees were killed by fire. Whether these types
will undergo conversion to longleaf pine forest with continued burning
depends on changes in species composition in newly recruited seedlings
and saplings, particularly the successful establishment of longleaf pine
seedlings. In the current landscape, wherever the longleaf pine is still
dominant, it is not difficult to change the structure and appearance of
that particular vegetation type. However, at sites where the longleaf
pine once was present but is now rare, such as some sandhills and upper
slopes, conversion to longleaf pine forest by means of prescribed burn¬
ing will be more difficult. For the midslope and lowerslope types, the
intact canopy and low flammability may portend little change in the
understory and future regeneration; the lack of response to fire is
consistent with the idea that mixed pine-hardwood occurred on such sites
in the presettlement landscape (Marks & Harcombe 1981; Harcombe et
al. 1993).

In this study, modification of vegetation by fire was limited to the dry
end of the topographic-moisture gradient, and so the hypothesis of
differential fire effects is supported. The effect of fire on current
vegetation is conditioned by that vegetation, which is influenced by site
characteristics. This is consistent with a growing body of literature (e.g.,

332

THE TEXAS JOURNAL OF SCIENCE- VOL. 56(4), 2004

Platt et al. 1989; Gibson et al. 1990; Glitzenstein et al. 1995; 2003;
Breininger et al. 2002; Drewa et al. 2002). The results are also consis¬
tent with evidence that present patterns and trends in natural vegetation
in the Big Thicket area are strongly influenced by soil factors, site
history, and fire (Marks & Harcombe 1981; Streng & Harcombe 1982;
Liu 1992; Harcombe et al. 1993; Lin et al. 2004). This work supports
an approach to prescribed fire that recognizes natural patterns and
natural variation in fire intensity, and thereby promotes the natural
diversity of communities and the complexity of the vegetation for which
the region is famous.

Acknowledgments

We are grateful to Chet Cain, Gary Cox, Linda C. Kaiser, Julie
Swindell, and Rebecca McCulley for their assistance in the field, and
David McHugh of the Big Thicket National Preserve and Ike
McWhorter of The Nature Conservancy for directing prescribed burn¬
ing. Special thanks are due to Dr. Katherine B. Ensor and Dr. Joe
Ensor of Rice University for their assistance in statistical analysis, and
to Jeff Glitzenstein and Donna Streng for their assistance in developing
the rationale for this study and in reviewing the manuscript. This
research was sponsored by the National Park Service and by The Nature
Conservancy. This manuscript is derived from part of the senior
author’s Ph.D. dissertation at Rice University.

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PAH at: harcomb@rice.edu

TEXAS J. SCI. 56(4):335-346

NOVEMBER, 2004

GROWTH OF CHINESE TALLOW TREE {SAPIUM SEBIFERUM)
AND FOUR NATIVE TREES UNDER VARYING WATER REGIMES

Bradley J. Butterfield*, William E. Rogers
and Evan Siemann

Department of Ecology and Evolutionary Biology
Rice University, Houston, Texas 77005
* Current address:

School of Life Sciences, Arizona State University
Tempe, Arizona 85287

Abstract.— Abiotic stress tolerance may play a role in the invasion and spread of Chinese
tallow tree ( Sapium sebiferum). A greenhouse experiment was conducted to determine the
effects of water stress on the growth of Sapium and four tree species native to the south¬
eastern United States. Species identity, water treatment, and their interaction significantly
influenced growth rate and mass of seedlings. No native species had as high an average
growth rate as Sapium. Indeed, Sapium had a higher growth rate than every native species
in every water treatment with the exception of a single native species ( Liquidambar
styraciflua L.) in the drier treatments (pulse drought, well watered). Sapium exhibits the
potential to thrive at any point along the water gradient present in southeastern floodplain
forests .

Plant species distributions often reflect abiotic conditions. Species
composition may shift along a resource gradient based on efficiency of
resource use at different concentrations (Tilman 1982; 1985; Huston &
Smith 1987). Species distributions in some landscapes are based pri¬
marily on one resource, and in such cases analysis of the performance
of species along a gradient of that resource can be useful in predicting
community composition (Tilman 1987). Similarly, comparisons of the
performance of an invasive species and native species along a gradient
of the most limiting abiotic factor in an ecosystem may be a good
predictor of the conditions in which the invasive will displace natives
(Alpert et al. 2000; Sakai et al. 2001; Daehler 2003).

Invasive species often have very different ecological attributes from
species in their introduced range (Bruce et al. 1997; Busch & Smith
1995). Comparisons between native and exotic congeners (Schierenbeck
et al. 1994; Mack 1996; Gerlach & Rice 2003) and between ecologically
similar native and exotic species (Nijjer et al. 2002; Rogers & Siemann
2002; Daehler 2003; Siemann & Rogers 2003a) have produced informa¬
tive results. Studies analyzing plant growth along a resource gradient
can be useful for identifying traits that may lead to the competitive
dominance of invasive species, as well as for predicting potential range
expansions.

336

THE TEXAS JOURNAL OF SCIENCE— VOL. 56(4), 2004

In southeastern floodplain forests, water is a major determinant of the
distribution of tree species (e.g. Hall & Harcombe 1998; Wall & Darwin
1999; Denslow & Battaglia 2002; Ernst & Brooks 2003). The elevation-
al heterogeneity of these systems positions different plant communities
within close proximity to each other (Christensen 2000), which likely
results in distribution of propagules into a wide range of moisture
conditions, making seedling establishment and growth important aspects
of population dynamics. Sloughs and depressions are often flooded year
round, while other areas of bottomland forests experience seasonal
flooding. Upland areas may never flood, and often experience seasonal
droughts (Christensen 2000).

Tree species in these forests can be expected to follow different
growth strategies depending on their distribution along a water gradient.
Stress tolerance is important at extreme elevations where abiotic factors
limit seedling growth and survival, while competitive ability is more
important in less stressful environments. Stress tolerant species are
expected to have relatively restricted phenotypic responses to external
stimuli since survival depends on highly conservative growth strategies
(Grime 1974; 1977; Campbell & Grime 1992). This is often reflected
in slow growth rates and negligible increases in mass and growth rate in
less stressful conditions (Grime 1974; 1977; Pigliucci 2001). Tree
species adapted to more favorable conditions can be expected to maxi¬
mize resource assimilation and grow rapidly, since biotic competition is
often more important than in stressful environments (Grime et al. 1986).

A greenhouse experiment was conducted to determine the growth and
performance of Sapium sebiferum (L.) Roxb. (Chinese tallow tree) and
four native tree species under a range of water conditions representative
of natural conditions. Sapium has invaded a variety of ecosystems in the
southeastern United States. Even though it thrives in early successional
conditions and has extremely high growth rates (Siemann & Rogers
2003a), seedlings are also shade tolerant (Jones & McLeod 1989; Rogers
& Siemann 2002; 2003; but see Lin et al. 2004) and flood tolerant
(Jones & Sharitz 1990; Conner et al. 1997, 2001).

It was predicted that the range of soil moisture conditions in which
native tree species sustain high growth rates and mass production would
be restricted. Adaptations to particular habitats were expected to cause
tradeoffs between stress tolerance and other traits such that native
species with the greatest growth rates in optimal conditions should be

BUTTERFIELD, ROGERS & SIEMANN

337

more sensitive to extreme conditions. Because of its widespread distri¬
bution in floodplain forests and invasive nature, Sapium was expected
to have a higher growth rate and produce more mass than all native
species under all water conditions.

Methods

The experiment was conducted in a climate controlled greenhouse in
Houston, Texas between March and August 2003. The roof and walls
of the greenhouse were clear glass, and humidity was approximately
100%. Pinus taeda L. (loblolly pine), Liquidambar styraciflua L.
(sweetgum), Nyssa aquatica L. (water tupelo), and N. sylvatica Marsh,
var. sylvatica (blackgum) seeds were acquired commercially (Louisiana
Forest Seed Co. Lecompte, LA). Sapium sebiferum seeds were collect¬
ed in Texas and Georgia. In Texas, seeds were collected from many
different trees at the Armand Bayou Nature Center, approximately 35
km southeast of Houston. In Georgia, seeds were collected from numer¬
ous trees on Sapelo Island, a barrier island approximately 55 km south
of Savannah. Seeds of all species were germinated in topsoil in early
March and transplanted into individual 11 liter plastic pots in April.
Potted seedlings of each native species plus one of Texas and Georgia
Sapium were assigned to a random position in each of twenty-four 160
liter plastic tubs (a split-plot design). Seedlings were watered daily for
two weeks before initiation of the treatments.

Each tub was randomly assigned one of four watering treatments,
with 6 tubs per water treatment. The treatments were: (1) Control -
Pots were watered daily until water flowed out of the bottom of the pot;

(2) Flooded - Pots were permanently submerged in water (1-3 cm above
soil surface) for the duration of the 16- week experiment. Evaporative
losses were replaced with de-ionized water to avoid salt accumulations;

(3) Pulsed flood - Pots received the control water treatment for two
weeks followed by flood treatment for the following two weeks. This
four-week cycle was completed four times during the course of the
experiment; (4) Pulsed drought - Pots received the control water treat¬
ment for the first two weeks of each four- week cycle, but received no
water for the latter two weeks.

Initial stem heights, basal diameters, and leaf counts were recorded
for each plant on 9 April. Stem height and number of leaves per
seedling were measured weekly during the experiment. After 16 weeks,
all of the plants were harvested. Roots, stems, and leaves were separ¬
ated and dried at 60 °C for 96 hours before dry mass was measured.

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THE TEXAS JOURNAL OF SCIENCE— VOL. 56(4), 2004

Figure 1 . Dependence of the growth rate of each tree species on water treatment (mean + 1
SE). Letters indicate significantly different means (P<0.05) within (lowercase) and
among (uppercase) species. The mean growth rate across all species and treatments is
provided as a reference.

All statistical analyses were conducted in SAS Version 8 (SAS
Institute 1999). ANOVAs were performed using PROC MIXED to
analyze the effects of species identity (split-plot factor), water treatment
(whole-plot factor) and their interaction (split-plot factor) on growth rate,
total biomass, and mass allocation. Stem growth rate was measured as
In (final height/initial height). Total mass was log transformed for
analyses. Proportion of total mass allocated to root, stem, and leaf
tissues were measured as organ mass/total mass. Fisher’s Least Signifi¬
cant Difference (LSD) was used for means contrasts among treatments.

Results

Stem growth rate depended on species (F5 >100 = 124.5; P< 0.0001),
water treatment (F3 20 — 99.1; P< 0.0001), and their interaction (F3j100
= 18.3; P< 0.0001; Fig. 1). Georgia Sapium grew most rapidly, fol¬
lowed by Liquidambar, Texas Sapium , N. aquatica, N. sylvatica , and
Pinus (Fig. 1). Georgia Sapium varied the least in growth across water
treatments (1.34- fold difference between treatment in which it grew
fastest and the one in which it grew slowest), followed closely by N.
aquatica (1.49-fold) and Texas Sapium (1.65-fold), then Pinus (2.17-
fold), Liquidambar (4. 34- fold), and N. sylvatica (9. 00- fold).

BUTTERFIELD, ROGERS & SIEMANN

339

«s

Species

Figure 2. Dependence of total mass of each species on water treatment (mean +1 SE).
Letters indicate significantly different means (P < 0.05) within (lowercase) and among
(uppercase) species. The mean total mass across all species and treatments is provided
as a reference.

Total mass depended on species (F5A00 = 893.8; P<0.0001; Fig. 2),
water treatments (F3 20 = 1 17.7; PcO.0001), and their interaction (F3 100
= 24.2; P< 0.0001; Fig. 2). Nyssa aquatica and Texas Sapium had the
highest total mass (Fig. 2), but N. aquatica seedlings were on average
between two and four times as tall as the other species at the beginning
of the experiment, which likely contributed to the high final mass (Fig.
3). In a split-plot design these differences in starting sizes are difficult
to account for with covariates. Texas Sapium had a slightly larger final
mass than Georgia Sapium , but this can also be reconciled by initial
heights (Fig. 3). Liquidambar and N. sylvatica were both significantly
lower than Georgia Sapium but were similar with respect to each other.
All species but Pinus exhibited significant reductions in total mass in
response to permanent flooding (Fig. 2).

Proportion of total mass allocated to roots depended on species
identity (F5l00 = 81.4; PcO.OOOl) but not on water treatment (F3 20 =
1.2; P = 0.35) or their interaction (F3 100 = 1.8; P = 0.10). Propor¬
tional leaf mass depended significantly on both species identity (Fs wo =
198.6; PCO.0001) and water treatment (F320 = 5.54; PcO.Ol) but not
on their interaction (F3 100 = 0.46; P = 0.94). Stem mass proportion

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THE TEXAS JOURNAL OF SCIENCE— VOL. 56(4), 2004

(/)

1 -

Sap TX

Pinus.

N.a

Sapium GA

Sapium TX

□

Liquidambar

N. aquatica

N. sylvatica

Pinus

~r—

~ i —

— r-

Initial Height (cm)

Figure 3. Initial height at planting versus log (total mass) for each species.

— i

was significantly affected by species identity (F5 100 = 349.2; P< 0.0001)
and the interaction between species identity and water treatment (F3 100
= 15.1; P< 0.0001), but not water treatment alone (F3 20 = 0.7; P =
0.54). Sapium seedlings allocated approximately 30% of mass to leaves,
30% to stems and about 40% to roots. Nyssa aquatica had a root to
shoot ratio similar to Sapium , but allocated markedly less mass to
leaves. Liquidambar and N. sylvatica were similar to each other in their
stem versus leaf allocation ratios, but N. sylvatica had the highest root
to shoot ratio of any species, while Liquidambar allocated a relatively
low amount of mass belowground. Pinus had the lowest root to shoot
and stem to leaf ratios (Table 1).

Discussion

The results of this experiment suggest that Sapium has characteristics
of both stress tolerant and rapidly growing species without experiencing
the same magnitudes of tradeoffs between these characteristics as are
evident for the native tree species in this study. Sapium had high
growth rates across all water treatments and experienced only modest

BUTTERFIELD, ROGERS & SIEMANN

341

Table 1. Proportion of total mass allocated to root, stem, and leaf parts by species.

Species

% Total Mass

Root

Stem

Leaf

Sapium GA

Sapium TX

Liquidambar

Nyssa aquatica

Nyssa sylvatica

Pinus

reductions in growth in response to water stress (Figs. 1,2). Sapium' s
stress tolerance appears to extend across the entire experimental water
gradient. Within this range of tolerance, Sapium' s growth rate was
always high relative to most native species. The only species that grew
faster than Sapium was Liquidambar in drier treatments, and it was a
very poor performer in the flood treatment (Fig. 1).

While Sapium may not be able to out perform N. aquatica in perma¬
nently flooded conditions if differences in initial seedling sizes observed
here are typical of field conditions (Fig. 2), Sapium seedlings may still
survive to reproductive maturity due to relatively low competition in
such stressful environments (Ernst & Brooks 2002). The high leaf-to-
stem mass ratio of Sapium relative to N. aquatica also indicates that
Sapium may be able to survive in very wet areas with dense canopies in
which N. aquatica may not be able to capture enough light to grow well
(Jones & Sharitz 1990). Sapium should also be able to exist in the
middle-to-high moisture range of Liquidambar and N. sylvatica. In
areas that are highly favorable for either of the natives, Sapium' s shade
tolerance (Rogers & Siemann 2002; 2003) and ability to reproduce as a
sub-canopy species may favor its presence. The performance of Sapium
in areas with drier moisture regimes was not tested in this study, but it
has been shown to be much less successful in dry uplands that support
Liquidambar and N. sylvatica (Hall & Harcombe 1998; Harcombe et al.
2002; Lin et al. 2004).

Sapium also exhibited positive traits similar to Liquidambar and N.
sylvatica. High growth rates in non- flood treatments (Fig. 1) and high
leaf-to-stem ratios (Table 1) of these two natives are indicative of
seedlings adapted to relatively nutrient-rich, disturbed areas (Grime
1974; 1977). Nyssa sylvatica had high root : shoot ratios (Table 1) and
relatively greater mass production in flood treatments (Fig. 2) indicating
that seedlings of this species may survive periods of flooding and grow

342

THE TEXAS JOURNAL OF SCIENCE— VOL. 56(4), 2004

rapidly when floodwaters subside (Grime et al. 1986). Liquidambar
performed as a more typical gap species, allocating more resources to
stem growth rate in a relatively narrow range of dry to moist soils (Fig.
1, Table 1). Sapium exhibited growth traits that were characteristic of
these two native species including high root to shoot ratios, intermediate
leaf to stem ratios, and high growth rates (Table 1).

The potential gradient distributions of native seedlings in this experi¬
ment corresponded relatively well with observed distributions of mature
trees. Nyssa aquatica was clearly the most tolerant of both flood treat¬
ments. Mature N. aquatica trees often coexist with Taxodium distichum
(L.) Rich, as the dominant species in anoxic bottomlands (Marks &
Harcombe 1981; Visser & Sasser 1995). Nyssa sylvatica seedlings can
likely survive periodic flooding while taking advantage of intermittent
dry periods, as well as thrive in moist areas. Distribution of mature
individuals of this species also covers a wide range of moisture condi¬
tions, including areas with seasonal flooding and drought (Keeland et al.
1997). Liquidambar performed best in moist to dry conditions, which
does appear to deviate slightly from the observed distribution of mature
trees. Liquidambar is primarily a floodplain species (Marks &
Harcombe 1981; Denslow & Battaglia 2002; Ernst & Brooks 2003), but
the drought treatment in this experiment was not severe enough to
simulate upland conditions. Therefore, dry conditions in this experiment
are similar to more elevated areas within a floodplain. Light may also
play an important role in the distributions of Liquidambar and N.
sylvatica. Their strategy of maximizing shoot growth in this study is an
adaptation consistent with these species being shade intolerant (Hall &
Harcombe 1998; Lin et al. 2004). The high variability of total mass and
mass allocation under varying water regimes also indicates that these
species maximize growth under relatively specific, favorable conditions.
Pinus was more flood tolerant in this study than was expected
(Kozlowski 1997) and was relatively incongruous with respect to distri¬
bution of mature trees. Light availability is another important predictor
of Pinus distribution in nature, which may explain this discrepancy
(Harcombe et al. 2002). The apparent flood tolerance may also be a
reflection of the fine-grained soils used in this study, which may have
stunted the growth of seedlings in all water treatments.

It is not clear what mechanism would contribute to the superior
performance of the invasive species observed in this study. One possi¬
bility is that Sapium possesses novel physiological or biochemical traits
as a result of taxonomic novelty or an evolutionary history in a different

BUTTERFIELD, ROGERS & SIEMANN

343

biotic province or under different selection pressures (Tilman 1999).
This possibility cannot be discounted. Sapium is unusual in that it is the
only tree in the southeastern U.S. that is a member of the Euphorbia-
ceae. In addition, Sapium is the only plant from Asia in this study, and
it is possible that in general Asian trees would outperform North
American trees in this type of experiment. Finally, Sapium has a long
history of being cultivated in Asia for its oil rich seeds, and was origin¬
ally introduced to the U.S. as an agricultural crop (Bruce et al. 1997).
The traits observed here could be the result of artificial selection prior
to introduction to North America. There are, however, proximate eco¬
logical factors that contribute to the success of invasive plants that may
have relevance to the results of this experiment.

Low herbivore loads in the introduced range is one of the factors that
is widely believed to contribute to the greater vigor of exotic plants
(Keane & Crawley 2002), and has been shown to contribute to Sapium' s
success (Rogers & Siemann 2002; Siemann & Rogers 2003a). One way
in which plants may benefit from low herbivore loads is by a plastic
phenotypic response to low losses to herbivores in which additional
resources are used for growth (Elton 1958). In this greenhouse study,
however, there was negligible damage to any plants, either natives or
Sapium , so this is unlikely to be the cause of Sapium' s unusual combina¬
tion of high growth rates and high flood tolerance observed here. In
fact, Liquidambar , the only species that was able to outperform Sapium
in this study, sometimes suffers extremely high herbivore damage in
natural settings (Siemann & Rogers 2003a) which would only strengthen
the conclusion that Sapium has an unusual combination of growth and
tolerance to stress.

Release from herbivory may also affect plant performance by direc¬
tional selection on plant defense and growth (Blossey & Notzold 1995).
Sapium' s high level of vigor in a wide range of conditions may be due
to genetic responses to low herbivory resulting in reallocation of re¬
sources from defense to faster growth (Siemann & Rogers 2001 , 2003b)
and perhaps also to phenotypic plasticity (Bazzaz et al. 1987, Alpert et
al. 2000). If this is true, the tradeoff between growth rates and stress
tolerance examined in this study may be applicable to plant responses
under varying conditions of other resources and other forms of stress.
Comparisons of the results of a greenhouse study such as this and
natural distributions may give insights into the role of other factors, such
as herbivory, in determining plant distributions.

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THE TEXAS JOURNAL OF SCIENCE— VOL. 56(4), 2004

This study adds further support to the importance of stress tolerance
in the invasion of southeastern floodplain forests by Sapium. The two
primary determinants of species distribution in these forests are light and
water (Hall & Harcombe 1998). Other studies have demonstrated
Sapium' s ability to grow in a variety of light levels (Jones & McLeod
1989; Rogers & Siemann 2002; 2003; Siemann & Rogers 2003c). In
accordance with other studies on soil moisture regimes (Jones & Sharitz
1990; Barrilleaux & Grace 2000; Conner et al. 2001), this experiment
confirms that Sapium can perform well under a wide range of water
conditions. Regardless of the mechanism, Sapium is able to exhibit
traits of both rapidly growing and stress tolerant species, which may
allow it to spread into bottomlands with anoxic soils as well as into
seasonally dry areas of floodplain forests. Perhaps more importantly,
this study demonstrates the ability of an introduced species to minimize
tradeoffs that substantially affect the performance and growth strategies
of native species.

Acknowledgments

We would like to thank Saara DeWalt for statistical assistance and
comments on the manuscript; Paul Harcombe and two anonymous
reviewers for comments on the manuscript; Candice Donahue, Maria
Hartley, and Somereet Nijjer for comments; Philemon Chow, Zac
McLemore, Rachel Tardif, and Terris White for assistance; Armand
Bayou Nature Center, University of Georgia Marine Institute and
Georgia Department of Natural Resources for permission to collect seeds
on their properties; the National Science Foundation (DEB-9981654) and
EPA (R82-8903) for support.

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Gerlach, J. D. & K. J. Rice. 2003. Testing life history correlates of invasiveness using
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BJB at: Bradley.J.Butterfield@asu.edu

TEXAS J. SCI. 56(4): 347-356

NOVEMBER, 2004

EFFECTS OF TEMPERATURE AND MULCH DEPTH ON
CHINESE TALLOW TREE (SAP1UM SEBIFERUM)

SEED GERMINATION

Candice Donahue*, William E. Rogers
and Evan Siemann

Department of Ecology and Evolutionary Biology
Rice University, Houston, Texas 77005
* Current address:

Armand Bayou Nature Center
PO Box 58828
Houston, Texas 77258

Abstract.— Shredding mowers can be used in prairie and savannah restoration to quickly
eliminate trees, such as the invasive Chinese tallow tree ( Sapium sebiferum), and leave a
layer of mulch on the ground. Sapium has shown highest germination rates in fluctuating
daily temperatures, and mulch has been shown to damp those fluctuations in the field. A lab
study was conducted to separate direct effects of mulch depth and indirect effects from
changes in soil temperatures on Sapium seed germination. Sapium seeds were exposed to
different combinations of mulch depth and temperature oscillations. Sapium seeds showed
highest germination in large temperature oscillation treatments regardless of the depth of the
mulch. Seedlings were able to emerge through mulch up to 10 cm deep, the maximum used
in this study. While herbicide use appears to be necessary because of resprouting from
stumps, this study indicates that mulching Sapium trees shows promise as a restoration tool
by removing existing trees as well as by reducing Sapium regeneration from seed through
the indirect effects of mulch on seed germination. The lower subsequent seedling numbers
might reduce the frequency and intensity of future herbicide treatments.

The invasive Chinese tallow tree ( Sapium sebiferum (L.) Roxb.),
Euphorbiaceae, was introduced to the United States from Asia in 1772
and has spread across the southeastern states (Barrilleaux & Grace 2000;
Bruce et al. 1997). Grasslands have always been subject to woody
encroachment, but the great seed output, bird dispersal, rapid growth,
and adaptation to wide environmental conditions of Sapium (Renne &
Gauthreaux 2000; Rogers et al. 2000; Siemann & Rogers 2003a) have
allowed it to become the most serious threat to endangered prairies along
the upper coast of the Gulf of Mexico (Grace 1998). Once Sapium
becomes established, it shades out the native herbaceous vegetation and
forms a monospecific forest (Bruce et al. 1997; Siemann & Rogers
2003b). This also displaces native animal species, such as several
federally endangered grassland birds (Herkert et al. 2003; Perkins et al.
2003). The loss of prairie bunchgrasses and rapid decomposition of
Sapium litter (Cameron & Spencer 1989) leave the soil bare beneath the
trees; such a condition may reduce bioremediation of anthropogenic

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THE TEXAS JOURNAL OF SCIENCE-VOL. 56(4), 2004

pollutants and speed the flow of water and sediments to rivers (Fajardo
et al. 2001; Harbor et al. 1995; Liaghat & Prasher 1996).

Sapium invasion is not limited to prairies. A 20-yr forest dynamic
study (Harcombe et al. 1999) revealed that Sapium had increased
dramatically in the Neches Bottom Unit of the Big Thicket National
Preserve between 1981 and 1995. Among small saplings, Sapium
growth was three times the median of all species studied during that
period, and among large saplings, Sapium growth significantly exceeded
that of all other species. In another study of the area, Hall & Harcombe
(1998) documented an interaction of shade tolerance and flood tolerance
among the species present. For example, species often were found in
higher light conditions than would be expected from their known
tolerance for shade, apparently having to make environmental trade-offs
to survive both stresses of shade and flooding. Since Sapium is known
to perform well in shade (Jones & McLeod 1989; Rogers 2002) and
withstand flooding (Conner 1994; Grace 1998), it may become a serious
threat to native tree species in the Big Thicket.

Effective control for Sapium has been elusive, and a great percentage
of coastal prairie has been displaced by this exotic species. A promising
new technique for prairie restoration uses shredding mowers to mulch
stands of Sapium. This method employs a large shredding mower to
chip entire trees at ground level. Herbicide is manually applied to the
cut surface of the stumps to reduce resprouting. For restoration to be
successful, Sapium regeneration needs to be controlled while simul¬
taneously promoting native prairie plant regeneration. Mulch from
Sapium trees may contribute to successful prairie restoration by limiting
Sapium regeneration from seed. However, mulch depths necessary for
suppression of Sapium seed germination and the mechanisms that contri¬
bute to suppression are not known.

Armand Bayou Nature Center, located 44 km southeast of Houston,
Texas, has twice mulched Sapium trees on invaded prairie with a
shredding mower, once in summer of 2000 and again in fall 2002/spring
2003. In the 2000 restoration, the stand was more mature and resulting
mulch depths ranged up to 15 cm. In the younger stand mulched in
2002/2003, average mulch depths were approximately 5 cm. The
subsequent emergence of Sapium seedlings in the area mulched in 2000
appeared lower than in the area where Sapium trees were killed with
herbicide and left standing.

DONAHUE, ROGERS & SIEMANN

349

The mulch layer might have reduced germination by limiting day /
night variation in surface soil temperatures. Experimental studies have
shown highly variable germination rates for Sapium , depending on the
geographic source of the seeds (Cameron et al. 2000) and the germina¬
tion protocols. Conway et al. (2000) only achieved 0-10% gemination
on filter paper in petri dishes under an oscillating light and temperature
regime, but Cameron et al. (2000) and Renne et al. (2001) achieved
26% and 22.5% gemination rates, respectively, for seeds planted in soil
in greenhouses under natural temperatures and light. Seeds under these
conditions would be expected to experience natural daily fluctuations in
soil temperatures. In another study, highest germination rates were
obtained for seeds planted in soil under experimentally controlled
fluctuating daily temperatures (Nijjer et al. 2002).

The objective of this lab study was to separate direct effects of mulch
and indirect effects by changes in soil temperatures on Sapium seed
germination by maintaining constant temperature regimes under varying
mulch depths. If direct effects of mulch on seed germination are the
primary cause of lower germination rates, then germination should
decrease as mulch depth increases for all temperature treatments. How¬
ever, if indirect effects via changes in soil temperatures are more
important, germination should be greatest in high oscillating tempera¬
tures regardless of the mulch depth.

Materials and Methods

Seeds of Sapium were collected from trees at the University of
Houston Coastal Center in Galveston County, Texas, from August to
September, 2002 and stored at room temperature. On 16 July 2003, 50
seeds were planted in each of 48 plastic bins (16 by 30 by 10 cm deep)
on a 2.5 cm layer of commercially available topsoil and covered with
another 2.5 cm layer of topsoil. Bins were randomly assigned to a
temperature treatment (high oscillation, low oscillation, warm, and cool)
and a mulch treatment (bare soil, 5 cm Sapium mulch, and 10 cm
Sapium mulch) in a full-factorial design. Temperature treatments were
chosen based on field soil temperatures measured during spring 2003 in
the field that was mulched in late 2002 (Fig. 1). Bins were in a
temperature controlled room (21 °C) without windows or artificial light
for the duration of the experiment. Sapium germination is independent
of light conditions (Nijjer et al. 2002).

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THE TEXAS JOURNAL OF SCIENCE— VOL. 56(4), 2004

Figure 1. Sample of field soil temperatures recorded every 30 minutes, by mulch depth, in
a field that had Sapium trees removed with a shredding mower in late 2002. Vertical bars
indicate midnight on successive days.

Electric roof de-icing cables (EASYHEAT, New Carlisle, IN) laid in
the bottoms of the bins raised the soil temperatures. Cables passed once
through low-oscillation bins and twice through high-oscillation and warm
bins. Oscillation treatments were warmed for 16 hours and allowed to
return to room temperature over eight hours. The high oscillation
temperature maximum was 33 °C, and the low oscillation temperature
maximum was 27 °C. The warm treatment was a constant 33 °C, and the
cool treatment was constant room temperature (21 °C).

Fresh Sapium mulch was collected from a recently mulched Sapium
restoration area at Armand Bayou Nature Center. Mulch was spread
evenly across the soil in the 5 cm and 10 cm mulch treatment bins.
Plastic baffles were used to support the mulch layer at the edges of the
10 cm treatment bins. Because the 0 cm and 5 cm mulch treatments lost
more heat to the air than the 10 cm mulch treatment and did not main¬
tain the desired soil temperatures, heavy-duty plastic sheeting was cut
slightly larger than each bin and laid over the tops of the bins for these
two treatments. The plastic was neither sealed to the bins nor in contact
with the soil or mulch layers.

DONAHUE, ROGERS & SIEMANN

351

Table 1 . Dependence of Sapium germination on experimental temperature and mulch depth
treatments in an AN OVA.

Factor

F- value

P-value

Temperature

112.2

123.5

<0.0001

Mulch Depth

2.0

3.4

<0.05

Temperature*Mulch

3.5

1.9

0.11

Error

10.9

All treatments were thoroughly watered three times each week until
water drained from the bins, and newly germinated seeds were counted
and removed from the bins during these periods. The experiment was
conducted for 125 days, but no seeds germinated after 110 days.

ANOVA was used to compare the different experimental treatments
and Fisher’s LSD tests were used for post-hoc means contrasts (Statview
5.0, SAS Institute, 1998, Cary, North Carolina). Data were checked for
normality and square root transformed to meet the assumptions of
ANOVA. Data were back- transformed for presentation.

Results

Temperature treatment and mulch depth treatment, but not their
interaction, had significant effects on seed germination; however,
temperature alone explained 87% of the variation in germination (Table
1). All pairwise comparisons among temperature treatments were
significantly different (P ranging from <0.0001 to 0.0152) with the
greatest germination in the high oscillation (217 germinants from 600
seeds total) followed by low oscillation (34 germinants), warm (18
germinants) and cool (1 germinant) treatments (Fig. 2). The only
significant difference among mulch treatments was the lower germination
rate under 5 cm of mulch compared to bare soil (Fig. 2).

Discussion

Germination success for Sapium clearly depends on daily fluctuations
in temperature, and the amplitude of the fluctuation is critical, as
evidenced by the magnitude of the difference between germinants in the
high-oscillation treatment and the low-oscillation treatment (Fig. 2).
Pioneer species and wetland species commonly use diurnal temperature
fluctuations as an indicator of canopy gaps (Fenner 1985; Baskin &
Baskin 1989), proximity to the soil surface (Thompson & Grime 1983;

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THE TEXAS JOURNAL OF SCIENCE-VOL. 56(4), 2004

Hi-Osc Lo-Osc Warm Cool

Temperature Treatment

Figure 2. Number of Sapium seeds germinating in each bin (means + 1 SE) for each
combination of temperature treatment (Hi-Osc = 21-33°C, Lo-Osc = 21-27°C, Warm
= constant 33 °C, Cool = constant ambient 21 °C) and mulch depth (0 cm, 5 cm, 10 cm).

Ghersa et al. 1992), or recession of standing water (Fenner 1985).
These environmental conditions are often critical to subsequent seedling
success (Thompson & Grime 1983; Fenner 1985; Vleeshouwers et al.
1995).

Several studies of invasive species have shown dependence on
temperature fluctuations for successful germination (Ghersa et al. 1992;
Lonsdale 1993; Young & Clements 2001). Also, several threatening
invasives are woody invaders of wetland areas, including Sapium (Davis
et al. 1946; Bruce et al. 1997), Schinus terebenthifolius Raddi, or
Brazilian peppertree (Wheeler et al. 2001; Hight et al. 2003), and
Melaleuca quinquenervia (Cav.) Blake, or punktree (Costello et al.
2003; Johnston et al. 2003). Mulching might be an effective control
method for other invasive woody species as well.

Germination and emergence from under 10 cm of mulch was not
significantly different from that from bare soil (P = 0.6575), and there
was no consistent trend in germination rates as mulch depth increased.
This supports a conclusion that the indirect effect of mulch on soil

DONAHUE, ROGERS & SIEMANN

353

temperature oscillations is more important than mulch depth alone for
Sapium seed germination. It is encouraging for the potential success of
this restoration method that only 5 cm of mulch in the field was required
to damp the soil temperature oscillations sufficiently (Fig. 1) to achieve
the germination suppression evidenced by the low oscillation treatment
in Figure 2.

The cotyledons of the seedlings in 10 cm of mulch were on long
attenuated stems. The large Sapium seed (0.16 g/seed, Bonner 1989)
apparently provides adequate resources for the seedling to emerge
through deep mulch before reaching light where it can begin to photo-
synthesize. Several studies in different environments have shown a
positive correlation between seed mass and ability for seedlings to
become established (Dzwonko & Gawronski 2002; Christie & Armesto
2003). When they modeled the emergence response of weed seeds to
burial depth, Grundy et al. (2003) also found that some species had
adequate reserves to emerge from a wider range of depths than might be
expected in the field, as Sapium demonstrated in the present study. This
may contribute to Sapium' s ability to invade and exploit many different
environmental conditions.

To be useful, the mulching treatment should have minimal effects on
native prairie species. Foster & Gross (1998) found that prairie forbs
and the prairie grass, Andropogon gerardi , were able to establish a
significant number of seedlings in intact plant litter, even though the
densities in litter were significantly lower than where litter was removed.
In multiple-site studies, Foster & Gross (1997) and Foster (1999) found
that accumulated litter affected Andropogon gerardi seedling establish¬
ment in some sites but not in others. Also, when examining tallgrass
prairie recolonization mechanisms after soil disturbance by pocket
gophers, Rogers & Hartnett (2001) found that vegetative regrowth after
burial under soil was the dominant recolonization mechanism. There¬
fore, possible mulch-induced seed germination suppression could be
expected to have little impact on native vegetation. Finally, the high
flotation rubber tires of the mulching equipment limit damage to the root
structure of existing perennial vegetation.

Techniques for control of invasive vegetation include biological,
herbicidal, mechanical, or some combination of these. While herbicide
use appears to be necessary because of resprouting from stumps
(Jubinsky & Anderson 1996), this study indicates that mulching live

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THE TEXAS JOURNAL OF SCIENCE— VOL. 56(4), 2004

trees can be an effective initial mechanical treatment that reduces
subsequent seedling numbers, and thereby reduces the frequency and
intensity of herbicide treatments.

Acknowledgments

The authors would like to thank Armand Bayou Nature Center for
mulch, the University of Houston Coastal Center for permission to
collect seeds, Brad Butterfield, Summer Nijjer, and Rachel Tardiff for
assistance in the lab, and Wray-Todd Fellowship, US EPA (R82-8903),
and US NSF (DEB-9981654) for financial support.

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TEXAS J. SCI. 56(4):357-368

NOVEMBER, 2004

THE EFFECT OF MYCORRHIZAL INOCULUM
ON THE GROWTH OF FIVE NATIVE TREE SPECIES AND
THE INVASIVE CHINESE TALLOW TREE ( SAPIUM SEBIFERUM)

Somereet Nijjer, William E. Rogers and Evan Siemann

Department of Ecology and Evolutionary Biology
Rice University, Houston, Texas 77005

Abstract. — Mycorrhizal fungi may play an important role in plant invasions, but few
studies have tested this possibility. Chinese Tallow ( Sapium sebiferum ) is an invasive tree
in the southeastern United States. An experiment was conducted to examine the effects of
mycorrhizal inoculation, fungicide application, and fertilization on the growth of Sapium and
five native tree species (Liquidambar styracif.ua , Nyssa sylvatica, Pinus taeda, Quercus alba,
and Q. nigra) that co-occur in forests in the Big Thicket National Preserve in east Texas.
Seedlings were grown in a greenhouse for twenty weeks under full factorial combinations of
mycorrhizal inoculum, fungicide, and fertilizer. Mycorrhizal inoculation increased Sapium
growth but caused zero to negative growth changes of the five native species. This suggests
that Sapium may gain unusual benefits from mycorrhizal associations. Liquidambar
styraciflua benefited from mycorrhizal inoculation only in fertilized conditions which
indicates that the potential advantage Sapium might gain from mycorrhizal associations may
vary with native species and soil fertility.

Mycorrhizal fungi form close associations with roots of plants in
which in exchange for fixed carbon, the fungi provide essential nutrients
to the plant (N, P) and may protect the plant from pathogens, support
helpful bacteria, enhance soil aggregation, assist in water transport and
gain, and stimulate plant growth through auxin production; these asso¬
ciations can vary from mutualistic to parasitic depending on soil fertility
levels (Harley 1968; Allen 1991; Johnson et al. 1997; Smith & Read
1997; Van der Heijden & Sanders 2002). It is possible that mycorrhizae
play a key role in temperate forest dynamics and community responses
by changing the outcome of competition and by influencing plant fitness
(Johnson et al. 1997; Van der Heijden & Sanders 2002). Little attention
has focused on how the existing mycorrhizal network of the introduced
range may facilitate the invasion of exotic plant species.

Sapium sebiferum (L.) Roxb, a native to central China, was intro¬
duced to Georgia in the late 18th century (Bruce et al. 1997). Although
present in Texas in the early 1900’s, Sapium did not become invasive
until the middle of the century and has only rapidly increased abundance
in the past two decades in mesic and hydric forests in the Big Thicket
National Preserve (BTNP) in east Texas (Harcombe et al. 1999). Re-

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THE TEXAS JOURNAL OF SCIENCE-VOL. 56(4), 2004

cent studies have shown that Sapium benefits from low herbivore loads
(Siemann & Rogers 2001; 2003ab; Rogers & Siemann 2002; 2003), but
Sapium appears to have unusually high growth rates even after account¬
ing for differences in aboveground herbivore impacts. Although a
release from belowground pathogens could explain the high growth rates
of Sapium , unusually large benefits from mycorrhizal associations are
also a factor that may contribute to Sapium* & invasive success.

Generalist mycorrhizae with low host specificity may be able to form
associations with invasive plants (Richardson et al. 2000). This associa¬
tion by itself would not create unusually high benefits, and thus could
not be itself responsible for invasive success, unless the invader could
utilize the mycorrhizae in a novel fashion (Richardson et al. 2000). The
combination of potentially novel mycorrhizal utilization and the short
co-evolutionary history exotic plants have with native mycorrhizal
mutualists suggests that these plants could receive unusually high bene¬
fits or extremely high costs their introduced ranges (Richardson et al.
2000) . Another way that exotic invaders could obtain benefits would be
to usurp native species’ existing mycorrhizal network connections, or
utilize neighbors’ nutrient pools with their own extraradical (soil
exploring) hyphae, thus parasitizing neighboring competitors through
enhanced nutrient uptake (Marler et al. 1999; Zabinski et al. 2002).
Only limited work to date has been done to examine how the existing
mycorrhizal network of the introduced range may influence the competi¬
tive ability of exotic invaders (Bray et al. 2003). Understanding how
Sapium utilizes mycorrhizal associations in its introduced range may help
explain the mechanisms underlying its invasion in the BTNP and in¬
crease general knowledge of the role of mycorrhizae in affecting plant
community dynamics.

A greenhouse experiment was conducted to test the effects of mycor¬
rhizal inoculation, fungicide application, and fertilization on the growth
of Sapium and five tree species native to the BTNP. If mycorrhizae
contribute to Sapium invasion, then the performance advantage of
Sapium compared to natives should be greater with mycorrhizal inocula¬
tion than without. To potentially decrease the performance advantage
of Sapium if mycorrhizal inoculation facilitates invasion, Rovral fungi¬
cide was applied (Gange et al. 1990; Ganade & Brown 1997). Fertiliza¬
tion is predicted to highlight plant alterations in mycorrhizal dependen¬
cies and mimic potential changes in field conditions. Fertilization is
predicted to decrease the effect of mycorrhizae on plant performance

NIJJER, ROGERS & SIEMANN

359

because carbon costs are not offset by benefits of nutrient gathering in
high fertility (Menge et al. 1978; Buwalda & Goh 1981; Hetrick et al.
1988; Hetrick 1991; Johnson 1993; Peng et al. 1993) and additionally
because the benefits plants receive from mycorrhizae may be less
valuable in higher fertility conditions (Koide 1991; Johnson 1993;
Johnson et al. 1997). In Flatland Hardwood Pine Forests of the Lance
Rosier Unit in the Big Thicket, which are equivalent to Lower Slope
Hardwood Forests found elsewhere, phosphorus tends to be in limited
supply (Marks & Harcombe 1981; Knox et al. 1995; BTNP 2003) be¬
cause of its difficulty to acquire at low levels and strong adsorption to
soil particles (Nye & Tinker 1977; Read 1991). However, nitrogen
deficiencies may limit growth of plants with non-mycorrhizal affiliations
because they can only absorb simple forms of N (Chalot & Brun 1998).
Together these predictions will begin to answer how mycorrhizae may
promote or hinder Sapium’s invasibility and ultimately alter the sur¬
rounding native community.

Methods

Seeds of five native tree species that are common in mesic and hydric
forests in the BTNP and may potentially be outcompeted by Sapium
sebiferum ( Liquidambar styraciflua L. [sweetgum], Nyssa sylvatica
Marsh [blackgum], Pinus taeda L. [loblolly pine], Quercus alba L.
[white oak], and Q. nigra L. [water oak]) were purchased (Louisiana
Forest Seed Company, Lecompte, LA) to ensure that seeds were from
uniformly healthy trees. Sapium sebiferum seeds were collected at
Armand Bayou Nature Preserve (Houston, TX). Stratification took
place in a 21 °C cold-room in January- February 2003. Germination of
non- surface sterilized seeds occurred in an unheated greenhouse on the
Rice University campus during March-May 2003. Germinated seeds
were planted in 66 mL Conetainers (Stuewe & Sons, Inc., Corvallis,
OR) filled with potting soil.

Forty-eight similarly sized seedlings of each species were selected
approximately two weeks after germination. All of the plants within
each species were randomly assigned to one of eight treatments in a
full-factorial experimental design with inoculation (yes or no) , fungicide
(yes or no) and fertilizer (yes or no) for a total of six replicates per
treatment. Roots were gently brushed free of soil and the soil was
retained. Roots were then dipped in either “Silva Dip” (Reforestation
Technologies International, Salinas, CA) which contained a total of eight
general endo- and ectomycorrhizal species ( Glomus intraradices , Glomus

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THE TEXAS JOURNAL OF SCIENCE— VOL. 56(4), 2004

aggregation , Glomus mossae , Pisolithus tinctorius , and four species of
Rhizopogon sp.) or distilled water. Excluding Rhizopogon sp., which
is primarily found in the northwestern United States, at least one of the
remainder of the endo- and ectomycorrhizal species listed would be
encountered by the focal tree species of this study in the field (Keeley
1980; Black et al. 1981; McIntosh et al. 1985; Weber & Smith 1985;
Walker & McLaughlin 1991; Metzler & Metzler 1992; Lewis & Strain
1996; Constable et al. 2001). After dipping, roots were covered with
the retained soil and transplanted into 3.8 liter Treepots™ (Stuewe &
Sons, Inc.) filled with a mixture of 2/3 potting soil and 1/3 perlite. Pots
were placed within blocks grouped by species on plastic pallets on the
greenhouse floor because of differences in germination times. Pots were
watered as needed and periodically rotated within species blocks to
minimize shading and location effects.

Fertilizer was applied four times in the course of the 20- week experi¬
ment in weeks 3, 7, 12, and 17. Application rates were equivalent to
4 g/m2 each of N, P and K per application. This mimics field regulation
standard rates. Nutrients were added as ammonium nitrate (N), super¬
phosphate (P), and potash (K) dissolved in 40 mL of distilled water.
Distilled water was added to non- fertilized controls.

Rovral® 4 Flowable Fungicide (Aventis CS, Bridgewater, NJ) was
applied three times in the course of the 20-week experiment in weeks 4,
10, and 16. Rovral, active ingredient iprodione, has been shown to
reduce mycorrhizal infection in plant roots and is a contact pesticide
with no known systemic action (Gange et al. 1990; Ganade & Brown
1997). Application rates followed recommendations for controlling
pathogenic root fungi (Aventis 2001).

Initial height of each seedling was measured. Initial heights were
taken before seedlings were dipped into either inoculum or a distilled
water control and as such did not require sterilization of equipment to
pre-empt transfer of inoculum between sources. At the end of 20
weeks, roots, leaves, and stems were harvested and dried at 60 °C for
at least 72 hours before weighing.

An ANCOVA with starting height as a covariate was used to test
whether final mass (log transformed to achieve normality) depended on
experimental treatments in a model with all possible interactions among
experimental treatments (SAS 8.2, SAS Institute, Cary, NC). Mass data
were back transformed for graphical presentation. Single species
ANOVAs were used to investigate significant interaction terms in the full

NIJJER, ROGERS & SIEMANN

361

analysis and Fisher’s Least Significant Difference Test was used to test
for differences between treatment means (Stat View 5.0, SAS Institute,
Cary, North Carolina).

Results

The percent of root mass was independent of all factors other than
species (F5 238= 1 19.80, PC .0001). It was lowest for Pinus (29%)
followed by Liquidambar (40%), Q. nigra (46%), Sapium (47%), Nyssa
(53 %) and Q. alba (73 %). The contrasts among species were significant
at a =0.05 for all pairs of species except Q. nigra vs. Sapium . Because
allocation patterns are independent of treatments (modeled as a percent¬
age of belowground root biomass) and species is the only significant
factor explaining the allocation pattern variance, the remainder of the
analyses utilized total mass as the dependent variable.

Total mass varied among species (Table 1, Fig. 1) and the contrasts
among species were significant at a =0.05 for all pairs of species except
Q. alba vs. Nyssa and Liquidambar vs. Q. nigra. No other main effect
significantly affected mass in the ANCOVA (Table 1). Total mass
depended on starting height in the ANCOVA (Table 1). The species
which had significant correlations between starting height and log (final
mass) in z- tests were Q. alba (r=0.59, P< 0.0001) and Nyssa (r=0.41,
P< 0.001). Variation in mass depended on several interactions: species/
noculation, species/fertilization, species/inoculation/fertilization, and
species/inoculation/fungicide. Since each interaction term had species
as one of the factors, individual species ANOVAs were used to help
identify the main factors influencing the interactions.

The significant effect of species/inoculation in the full model indicat¬
ed that species differed in the direction or magnitude of their responses
to inoculation. All five native species tended to have lower mass when
inoculated but this difference was significant only for Nyssa (P<0.01)
in single species ANOVAs. Sapium had significantly higher mass when
inoculated (P< 0.01). In a separate analysis with a two-level predictor
that indicated whether a species was native vs. Sapium , the interaction
of this term and inoculation was significant (P<0.05).

The significant effect of species/fertilization in the full model
indicated that species differed in their responses to fertilization. In
single species ANOVAs, Pinus fP<0.01) and Liquidambar (P< 0.05),

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THE TEXAS JOURNAL OF SCIENCE-VOL. 56(4), 2004

Table 1 . The dependence of log(fmal mass) on experimental treatments in an ANCOVA with
starting height as a covariate. Significant terms are noted with an asterisk (*).

Factor

F-Value

P- Value

Species*

48.2

157.7

<0.0001

Fertilizer

0.1

1.6

0.20

Fungicide

0.0

0.2

0.70

Inoculum

0.1

0.9

0.35

Species/Fertilizer*

0.8

2.6

<0.05

Species/Fungicide

0.6

1.9

0.10

Species/Inoculum*

1.3

4.4

<0.001

Fertilizer/Fungicide

0.0

0.3

0.58

Fertilizer/Inoculum

0.1

0.9

0.34

Fungicide/Inoculum

0.0

0.5

0.48

Species/Fertilizer/Fungicide

0.3

0.9

0.50

Species/Fertilizer/Inoculum*

0.8

2.7

<0.05

Species/Fungicide/Inoculum*

0.8

2.7

<0.05

Fertilizer/Fungicide/Inoculum

0.1

1.3

0.26

Species/Fertilizer/Fungicide/Inoculum

0.3

0.9

0.45

Starting height*

1.2

19.6

<0.0001

Error

238

14.5

but no other species, were significantly larger when fertilized (Fig. 1).
Pinus had larger mass in fertilized controls and maintained this increase
when inoculated. However, Liquidambar1 s growth had significant mass
increases with inoculation in the fertilized treatments only.

Single species ANOVAs show that the significant interaction of
species/fertilization/inoculation in the full model was related to the
idiosyncratic effect of these treatments on Liquidambar mass CP <0.01,
Fig. 1). Inoculation reduced Liquidambar mass in low fertility condi¬
tions but increased it in high fertility conditions.

The significant effect of species/inoculation/fungicide largely reflect¬
ed the distinct responses of Sapium to fertilizer and fungicide since the
interaction of these treatments was only significant for Sapium (P< 0.01)
in single species ANOVAs. Submodels showed fungicide-non-inoculated
plants to be significantly different from fungicide-inoculated plants and
contol (non-fungicided, non- inoculated) plants to be significantly differ¬
ent from fungicided- inoculated plants by Fisher’s Least Significant
Difference Test, respectively (P< 0.01, /><0.05). Specifically, Sapium
mass was lowest in the fungicide only treatment (average = 7.8 g)
followed by control (non-inoculated and non-fungicided), (15.1 g),
inoculation only (15.1 g), and finally the combination of inoculation and
fungicide (20.9 g).

NIJJER, ROGERS & SIEMANN

363

Liquidambar Nyssa Pinus Q. alba Q. nigra Sapium

Figure 1. The dependence of mass (g) of Liquidambar styraciflua, Nyssa sylvatica, Pinus
taeda, Quercus alba , Quercus nigra , and Sapium sebiferum seedlings on fertilization (con
= no fertilizer, fert = fertilized) and mycorrhizal inoculation after 20 weeks. Fungicide
treatments are not shown. See Table 1 for statistical results.

Discussion

Sapium' s striking positive growth response to mycorrhizal inoculation
(65% increase) differed markedly from the neutral to negative responses
of native tree species (Fig. 1). The magnitude of reductions in growth
of the five native tree species in response to inoculation ranged from
negligible ( Q . alba = 1% reduction, Q. nigra = 6%) or minor ( Pinus
= 17%, Liquidambar = 24%) to large and significant ( Nyssa = 46%)
but the direction of the response to inoculation was always negative.
Sapium was clearly able to gain large benefit from mycorrhizal associa¬
tions with a generalist mycorrhizal inoculum in conditions where natives
could not. It appears that natives were unable to benefit from the
generalist inoculum in this study suggesting that mycorrhizal specificity
is important (Bever 2002; Klironomos 2003). The strains used in this
study may not be beneficial in these conditions and may create an un¬
necessary obligate symbiosis with direct translations to decreases in
growth (Hetrick et al. 1988; Hetrick 1991). This supports the hypothe¬
sis that unusual relationships between the exotic Sapium and North
American mycorrhizae species, such as those in the inoculum, may
contribute to Sapium' s success as an invader.

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THE TEXAS JOURNAL OF SCIENCE— VOL. 56(4), 2004

There are a number of explanations for why lack of specialist mycor-
rhizae (Bever 2002; Klironomos 2003), which was predicted to be bene¬
ficial, appeared to be especially detrimental in fertilized treatments for
Nyssa, Pinus, Q. nigra and for the native species Liquidambar and
Nyssa in unfertilized treatments in this experiment. First, carbon drain
on host plants, which is well documented (Buwalda & Goh 1981;
Hetrick 1991; Johnson 1993; Peng et al. 1993; Graham et al. 1996) may
have exceeded the benefits of increased nutrients and/or water in these
relatively fertile, well-watered greenhouse conditions. Second, mycor-
rhizae in this experiment may have used carbon from plants largely for
respiration rather than increasing extraradical hyphae surface area and
increasing nutrient absorption (Peng et al. 1993; Graham et al. 1996).
Increases in maintenance respiration, as well as higher root construction
costs due to high lipid vesicle allocation, has been shown in P addition
experiments for Citrus volkameriana (Peng et al. 1993, Graham et al.
1996) and has been attributed to decreases in carbohydrate root exudates
from plants in highly fertilized soils (Johnson et al. 1997).

The unexpected results for fungicide and inoculation combinations, in
particular the effects on Sapium mass, were inconsistent with the expec¬
tation that seedlings in the two treatments, non- inoculated fungicide only
and inoculation plus fungicide, would be identical in size. This suggests
that fungicide applications were not an effective method of fungal
control. One possible explanation is that non-spore ingredients in the
mycorrhizal inoculum had phytotoxic effects on seedling growth in the
presence of fungicide. The reduction of Sapium mass by fungicide
application (without inoculum) might indicate that beneficial microbes
(phosphate-solubilizing microbes and plant growth-promoting bacteria)
were present in the potting soil which were killed by the fungicide
(Allen 1992). Alternatively, it might indicate direct toxic effects of
fungicide on Sapium. The recovery of Sapium growth with inoculation
in fungicide treatments suggests that the mycorrhizal inoculum was not
effectively suppressed and that mycorrhizae may be acting synergistically
with microbes in the fungicided soil that were not effective or prevalent
in the non- fungicided soil. One goal of this greenhouse experiment was
to develop methods that could be applied in field experiments. Further
work with direct assays of mycorrhizal and non-mycorrhizal fungi in
experiments with Sapium is needed to complete the identification of
reliable field methods and identify the cause of the seemingly anomalous
inoculation and fungicide result.

NIJJER, ROGERS & SIEMANN

365

The prediction of decreased response of all species to mycorrhizal
inoculation in high fertility environments was based on the assumption
that mycorrhizal carbon costs are not offset by the benefits of nutrient
gathering in conditions in which nutrients are abundant (Menge et al.
1978; Buwalda & Goh 1981; Hetrick et al. 1988; Hetrick 1991; Johnson
1993; Peng et al. 1993). The positive response of Liquidambar to
mycorrhizal inoculation only in fertilized conditions was opposite the
prediction that the benefit of mycorrhizal associations would be lower
in more fertile conditions (Fig. 1). Indeed, the reverse pattern observed
here suggests that there may be potential for strong competition for
nutrients between mycorrhizae or other soil microbes and plants in low
fertility environments that may counteract the potential benefit of mycor¬
rhizal associations in these conditions (Bardgett et al. 2003).

The strong benefit of mycorrhizal inoculation for Liquidambar in
some conditions (Figure 1) indicates that the competitive advantage
Sapium might gain from mycorrhizal associations may vary with native
species and soil fertility (Marler et al. 1999).

One theory explaining the success of invaders in their introduced
range is the Enemy Release Hypothesis. It predicts that invasives
experience a release from the pressures of the natural enemies in their
native range and can therefore allocate additional resources to growth
and reproduction (Alpert et al. 2000; Maron & Vila 2001; Keane &
Crawley 2002; Mitchell & Power 2003). However, little attention has
been given to belowground enemies. This experiment raises the possi¬
bility that the large size of Sapium in all conditions, although doing
better with inoculum than natives, (Figure 1) reflects presence of below¬
ground pathogenic fungi that more readily attack native tree species.

The results reported here would be more compelling with confirma¬
tion of mycorrhizal colonization and dependence by direct examination.
Further, it is imperative that these results be verified in field trials as
well as in experiments including competitive interactions between
species. Such experiments are currently underway to rigorously test the
preliminary conclusion presented here that interactions with soil mi¬
crobes play a role in Sapium invasions in east Texas forests.

Acknowledgments

We would like to thank: the National Science Foundation (DEB-
9981546) and a Wray-Todd Fellowship for financial support; Bradley

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THE TEXAS JOURNAL OF SCIENCE-VOL. 56(4), 2004

Butterfield, Philemon Chow, Saara DeWalt, Candice Donahue, Maria
Hartley, Catherine LaMaur, Rick Lankau, Zack McLemore, Jay Nijjer,
Rachel Tardiff, Emily Wheeler, and Terris White for assistance and
support; and Armand Bayou Nature Center for permission to collect
seeds, Paul Harcombe and two anonymous reviewers for their com¬
ments.

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SN at: somereet@rice.edu

TEXAS J. SCI. 56(4): 369-3 82

NOVEMBER, 2004

CHARACTERIZATION OF ARTHROPOD ASSEMBLAGE
SUPPORTED BY THE CHINESE TALLOW TREE (SAPIUM SEBIFERUM)

IN SOUTHEAST TEXAS

Maria K. Hartley, Saara DeWalt, William E. Rogers
and Evan Siemann

Department of Ecology and Evolutionary Biology
Rice University, Houston, Texas 77005

Abstract.— Arthropod abundance, species richness and trophic structure were measured
on the introduced species Chinese Tallow tree ( Sapium sebiferum (L.) Roxb.) in southeast
Texas. Samples were collected using sweep nets between June and October of 2001 . A total
of 811 individuals and 160 arthropod species were caught. Orders Diptera, Acari, and
Araneida were abundant on Sapium , while orders such as Thysanoptera, Neuroptera,
Orthoptera were present in much lower relative abundances. The order Hemiptera was
markedly low in abundance and species richness. Compared to available data on native
ecosystems, predators and detritivores were relatively abundant while herbivores and total
arthropod diversity were relatively low on Sapium. These results suggest that Sapium has
not yet acquired an insect fauna comparable to native plants in Texas.

Arthropods represent a significant proportion of faunal community
diversity and have vital roles in ecosystem functioning (Wilson 1992;
Price 1997). A number of ecosystem services are performed by
arthropods, such as nutrient recycling, seed dispersal, herbivory, and
pollination (Proctor & Yeo 1972; Petrusewicz & Grodzinski 1975;
Davidson & Morton 1981; Jones et al. 1994). Introduced plant species
have been shown to alter ecosystem functioning, reduce native diversity,
and promote extinction of native species (Vitousek 1986; Liebhold et al.
1995; Mack et al. 2000), and through changes in vegetation structure,
composition and host quality, they may affect arthropod assemblages.
Insect diversity is frequently correlated with the diversity of plants
(Schowalter 1995; Siemann 1998) and architectural complexity of a
habitat (Strong et al. 1984). When previously diverse habitats are
converted to monospecific stands of non- native plants, insect species
richness will often be lower.

Factors that influence arthropod colonization rates on introduced plant
species may affect subsequent community composition and structure.
Strong et al. (1984) suggested that taxonomic, phenological , biochemi¬
cal, and morphological similarities between introduced and native plants,
as well as geographic range, may influence how quickly introduced
plants are colonized by native arthropods. However, arthropod host

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choice is typically driven by physiological and behavioral adaptations in
response to host plant quality (Price 1997; Schowalter 2000). Host
plants considered low quality for arthropod growth and development, are
typically highly defended and/or nutritionally poor (Price et al. 1980).
Host choice usually divides herbivorous insects into two categories, gen¬
eralists and specialists (Feeny 1976). Generalists capitalize on the most
abundant and obvious resource, whereas specialists possess increased
efficiency but reduced resource choice (Feeny 1976; Brown 1984).
Therefore, generalist arthropods are thought to be more commonly
found on introduced plant species than native species (Strong et al.
1984; Lankau et al. 2004), but little empirical evidence supports this
assertion.

Sapium sebiferum (L.) Roxb. (Euphorbiaceae) also known as Triadica
sebifera, invades coastal tallgrass prairie, disturbed areas, and intact
floodplain forests in east Texas (Bruce et al. 1997). The enemy release
hypothesis has been used to explain the success of some introduced
species including Sapium (Elton 1958; Keane & Crawley 2002; Siemann
& Rogers 2003a). It asserts that alien species are introduced without
their co-evolved specialist herbivores and pathogens. This release from
natural enemies may give alien species a competitive advantage over
native plants (Elton 1958; Groves 1989; Lodge 1993; Tilman 1999).
Indeed, there is evidence that herbivore loads are lower on introduced
plant species than native species (South wood et al. 1982; Strong et al.
1984; Yela & Lawton 1997). Furthermore, biological control agents
can sometimes control alien plant populations (Goeden & Louda 1976;
Groves 1989). If the enemies release hypothesis is valid, insects may
play an important role in the invasion of Sapium.

The objective of this study was to characterize the arthropod
community by quantifying arthropod taxonomic richness and abundance
on a monospecific stand of Sapium , growing on a former coastal prairie
in southeast Texas, and comparing to data from native habitats in
southeastern Texas (Birch 1975; McFadden 1978; Cameron & Byrant
1999). It was predicted that: (1) fewer herbivore species would be
found on Sapium than in native communities if Sapium is avoided by
North American herbivores, and (2) the arthropod community structure
on Sapium would be different from that found in native habitats, as
Sapium has been present for a shorter time and is therefore less likely
to have acquired a full insect fauna.

HARTLEY ET AL.

371

Materials and Methods

Focal study species. —Originally from Asia, Chinese tallow tree
( Sapium sebiferum ) was introduced to Georgia in the late eighteenth
century and subsequently into Texas in the early 1900’s (Bruce et al.
1997). Sapium is a dominant invasive species in the southeastern United
States (Flack & Furlow 1996; Bruce et al 1997). Once established it can
form dense monospecific stands with little under story vegetation (Bruce
et al. 1997). It experiences low levels of herbivory in Texas (Siemann
& Rogers 2001; 2003a; 2003b) but the diversity and composition of
associated arthropods in Texas is not known.

Study site. — The study was conducted at the University of Houston
Coastal Center (henceforth known as UHCC), a 374 ha research area,
located 50 km SE of Houston, Texas. Most of the research site consists
of Sapium stands in areas that originally would have been tallgrass
prairie. This study was conducted in a monospecific Sapium stand that
was estimated to be 30 years old.

Sampling protocol. — This Sapium stand was sampled 16 times
between 8 June and 24 October 2001. The sampling frequency was
devised for taxa that emerge for only short periods and, or have short
life spans. On each sampling occasion, four samples were collected
randomly from Sapium. Each sample was collected along a 16 m
transect. Transects were selected for minimal undergrowth to minimize
the influence of other plant species on the focal arthropod community.
Each transect was sampled for arthropods using 30 swings of a sweep
net (15 inches diameter) that reached 5.8m into the canopy (see Siemann
1998 for comparisons of sampling methods affecting relative abundance
and species richness). Sampling was conducted at approximately the
same time of day and under similar weather conditions (dry and warm).

Arthropod identification.— Arthropod specimens were sorted under
magnification and identified to either species or morphospecies within
family or genus, and abundance, and trophic group was recorded by
taxon. Individuals from the order Araneida (spiders) were often not
identified beyond order due to their taxonomic complexity and lack of
a local reference collection. Morphospecies have been shown to
correlate with arthropods identified by entomologists (Oliver & Beattie
1996), and this technique is often effectively utilized in the characteriza¬
tion of communities (Ingham & Samways 1996; Siemann 1998; Symstad
et al. 2000).

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THE TEXAS JOURNAL OF SCIENCE-VOL. 56(4), 2004

Determination of trophic level.— For each species or morphospecies,
a trophic group was determined for the developmental stage at which the
individual was caught by referring to relevant literature (Arnett 1960
1993; Borror & White 1970; McAlpine et al. 1981; 1987; Schuh &
Slater 1995). The functional groups were the following: herbivore,
detritivore, predator, parasite, omnivore, non- feeding, and unknown.
Herbivores included any arthropod feeding primarily on living plant
material. Omnivores were defined as individuals feeding on plants and
animals. The group ‘unknown’ was assigned for those whose trophic
grouping could not be determined through lack of available knowledge
or insufficient taxonomic determination. Little is known about feeding
habits for some taxonomic groups, especially those without agricultural
or medical importance. There are some arthropods that only feed in
their larval stage; therefore, a non- feeding group was included.

Data from previous studies.— The native sites and habitats sampled by
Cameron & Byrant (1999) were located near Sealy, Texas, approximate¬
ly 1 10 km NW of the Sapium study site (UHCC). They sampled using
a beating net for woody areas and a sweep net in herbaceous vegetation.
The beating nets usually have heavier canvas fabric that collects smaller
individuals than a sweep net. The habitats included: riparian woodland
with ungrazed pasture and savanna woodland (RW1), dense riparian
woodland with less open grassland (RW2), bottomland woodland with
dense herbaceous understory (BW3), fluvial woodland with open under¬
story with periodic flooding and bordered by pasture (FWP4), dense
drier woodland with woody understory (DW5), grazed pasture with a
few woody species (GP6), abandoned pasture with patches of riparian
woodland (PW7), and coastal prairie with no woody vegetation,
surrounded by agriculture and grazing (CP8). Cameron & Byrant
(1999) did not include non-insect arthropods in their study so these
groups were excluded from the UHCC data (including Sapium data) for
comparative analyses.

Two studies from UHCC on arthropod communities were also
included in this study (Birch 1975; McFadden 1978). Arthropod data
from high (HDB) and low densities (LDB) of Baccharis halimifolia L.
were utilized from an earlier study by Birch (1975). Like Sapium ,
Baccharis is both common and woody, yet Baccharis is native to the
area. Birch (1975) sampled the stands on four occasions in 1975, using
a D-vac. Siemann (1998) found that relative richness and abundance
values for D-vac and sweep net samples were strongly correlated.
McFadden (1978) collected arthropod data in the coastal prairie at

HARTLEY ET AL.

373

UHCC (UHCP) every two months, a total of seven times in the year,
using a sweep net. Sampling effort was standardized for McFadden
(1978), Birch (1975), and Cameron & Byrant (1999) by using relative
rather than absolute values. Birch (1975) and McFadden (1978) are the
only available studies on arthropod communities at the UHCC.

Data analyses. — To assess the differences in the Sapium insect com¬
munity from those in native Texas habitats, a non-metric multidimen¬
sional scaling (NMS) ordination was conducted using relative abundance
of seven insect orders from Sapium, high and low densities of Baccharis
(Birch 1975), coastal prairie (McFadden 1978), and eight native sites
studied by Cameron & Bryant (1999). Araneida and Acari were ex¬
cluded. NMS is a non-parametric, iterative technique based on ranked
distances among sites (McCune & Grace 2002). The number of dimen¬
sions was determined by a minimal stress (departure from monotonicity) .
The distance matrix of sites used for ordination was 1-DS, in which Ds
is Sorensen’s similarity index. Using the distance matrix output by
PC-ORD Version 4, the distance ordination was conducted in SAS V.8
(SAS Institute 2000) with routine PROC NMS.

Results

A total of 811 individuals and 160 species in 15 orders of arthropods
were caught in a total of 1920 sweeps. Some orders were abundant on
Sapium , such as Acari (mites), Araneida (spiders), and Diptera (flies),
which accounted for 78% of the individuals in the community (Table 1).
The most diverse orders were Diptera (36% species richness) and Acari
(13% species richness). Coleoptera (beetles), Homoptera (leafhoppers) ,
Hymenoptera (wasps and ants) and Psocoptera (barklice) were less
abundant on Sapium. Eight orders were rarely encountered (Collembola
(springtails), Dictyoptera (mantids and cockroaches), Ephemeroptera
(mayflies), Hemiptera (true bugs), Lepidoptera (moths and butterflies),
Neuroptera (lacewings), Orthoptera (grasshoppers and crickets), and
Thysanoptera (thrips). Twenty immature individuals were caught, of
which 13 were Orthoptera, and the remainder were Coleoptera, Homop¬
tera, and Thysanoptera.

A species accumulation curve was constructed to determine the
number of species collected versus sampling effort for the data on
Sapium. Three saturating equations were fitted to the curve (Tablecurve
2D, Systat, Point Richmond CA). They indicated that the total number
of species in the community was 189 (first order intermediate kinetic

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THE TEXAS JOURNAL OF SCIENCE- VOL. 56(4), 2004

Table 1 . Abundance and species richness of arthropods by taxonomic order summed over
all samples.

Order

Abundance

Species Richness

Acari

165

Araneida

248

—

Coleoptera

Collembola

Dictyoptera

Diptera

222

Ephemeroptera

Hemiptera

Homoptera

Hymenoptera

Lepidoptera

Neuroptera

Orthoptera

Psocoptera

Thysanoptera

TOTAL

811

160

function), 191 (simple equilibrium, net rate and equilibrium concentra¬
tion function), or 208 (first order intermediate kinetic function with
equilibrium) which suggests the sampling effort on Sapium caught 85%,
84%, or 77% of the species respectively. A species-sweep curve con¬
structed by McFadden (1978) showed that 1000 sweeps would contain
85% of the diversity. Cameron & Byrant (1999) also estimated they
collected 85% of the diversity (based on McFadden 1978). Birch (1975)
did not create a sampling curve.

The most abundant family encountered was Oripodidae (beetle or
armored mites), which accounted for 14% of total arthropod community
abundance (Table 2). Chironomidae (non-biting midges), Lauxaniidae
(Lauxaniid flies), and Dolichopodidae (long legged flies) were also
relatively common (Table 2). The most diverse (species rich) among
these were Dolichopodidae and Chironomidae. Other common families
were Psocidae (common barkl ice), Sciaridae (dark winged fungus gnats),
Formicidae (ants) and Coccidae (scales) (Table 2).

Only two families were encountered that might be considered as
specialist herbivores. These were Coccidae (scales) and Cicadellidae
(leafhoppers) both in the order Homoptera. Homoptera are often known
to stay on host plants where their eggs are laid.

Predators (326 individuals) and detritivores (241 individuals) together
represented 70% of the arthropod assemblage supported by Sapium.
Herbivores were considerably less abundant and composed only 7 % of

HARTLEY ET AL.

375

Table 2. Fifteen most abundant families sampled from Sapium. The families listed account
for 53% of total arthropod community abundance and 55% of total species richness.

Order

Family

Abundance

Species

Richness

Acari

Oripodidae

115

Diptera

Chironomidae

Diptera

Lauxamidae

Diptera

Dolichopodidae

Psocoptera

Psocidae

Diptera

Sciaridae

Hymenoptera

Formicidae

Homoptera

Coccidae

Homoptera

Cicadellidae

Hymenoptera

Braconidae

Diptera

Chloropidae

Orthoptera

Gryllidae

Neuroptera

Chrysopidae

Psocoptera

Pseudocaeciliidae

Coleoptera

Coccinellidae

all Sapium community arthropods (58 individuals). Insect relative
abundance for the additional trophic categories were 3 % for omnivores
and parasites, 10% unknown, and 8% non- feeding on Sapium. How¬
ever, species richness was more evenly proportioned among the trophic
categories. Detritivores were the most species rich (43 species or
morphospecies) but only represented 27% of the community diversity.
Both herbivores and predators had similar levels of diversity, represent¬
ing 20% and 17% respectively.

The arthropod community on Sapium differed from the communities
found on native sites sampled by Birch (1975), McFadden (1978), and
Cameron & Byrant (1999) (Table 3). After Acari and Araneida data
were removed, relative species richness and abundance were recalculated
to make all the data sets comparable. The relative richness of herbi¬
vores (29%) was approximately 50% less on Sapium than on native
vegetation (native herbivore range 49-67%). In contrast, both predator
and detritivore relative richness was higher on Sapium (24% and 38%
respectively) than the native site averages (12% and 16% respectively).
The average relative species richness for predators from native sites was
12% (range 6-19%), and the average for detritivores (native sites) was
16% (range 7-24%). Parasites on Sapium were similar in their relative
species richness (9%) compared to the native sites (range 8-21%).
Cameron & Byrant (1999) did not present results on the trophic distribu¬
tion of arthropod abundance.

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THE TEXAS JOURNAL OF SCIENCE— VOL. 56(4), 2004

Table 3. Arthropod relative species richness by trophic group for Sapium samples in this
study (“Sapium") and habitats sampled by Birch (1975), McFadden (1978), and Cameron
& By rant (1999). Refer to methods for description of sites.

Sites

Herbivore

Predator

Parasite

Detritivore

RW1

RW2

BW3

FWP4

DW5

GP6

PW7

CP8

UHCC prairie

HD Baccharis

LD Baccharis

Sapium

The comparison of community composition of Sapium and native sites
sampled by Birch (1975), McFadden (1978), and Cameron & By rant
(1999) showed both differences and similarities in the relative abundance
of orders (Table 4). Arthropod relative abundance on Sapium was
comparable within the range of relative abundance at native sites for
Homoptera, Coleoptera, Orthoptera, Hymenoptera, and Lepidoptera
(Table 4). However the relative abundance found on Sapium was higher
for Diptera and ‘others’, and lower for Hemiptera (Table 4).

The NMS ordination of relative abundance of orders indicated that the
insect community on Sapium differed substantially from that of native
sites (Figure 1). A 3-dimensional solution was found. However, a two
dimensional graph is presented, for ease of interpretation (Figure 1). A
total of 38 iterations were run for the final solution, and the final stress
was 0.08196. A final stress value between 0.1 and 0.05 is generally
interpreted as a good ordination with negligible risk of inferring false
conclusions (McCune & Grace 2002) . The UHCC sites were distinctly
separated from Cameron & Byrant’s (1999) sites along dimension 1
(Figure 1). The Sapium site was located at the extremes of both axes
(Figure 1). The grazed pasture site (GP6) was the most similar native
site to Sapium in insect community (Sorenson’s similarity index (SSI) =
0.75), followed by UHCC coastal prairie (UHCP) (SSI = 0.56), while
abandoned pasture with patches of riparian woodland (PW7) was the
most different (SSI = 0.31).

HARTLEY ET AL.

377

Table 4. Relative abundance of insects (Acari and Araneida excluded) by order from the
native habitats sampled by Birch (1975), McFadden (1978), Cameron & Byrant (1999),
and for Sapium samples in this study. These values are the percentage of each order
within each site. ‘Others’ include all other orders not already listed. Refer to methods
for site abbreviations. HOM = Homoptera, HEM = Hemiptera, COL = Coleoptera,
ORT = Orthoptera, DIP=Diptera, HYM = Hymenoptera, LEP = Lepidoptera.

Sites

HOM

HEM

COL

ORT

DIP

HYM

LEP

Others

RW1

13.2

39.0

33.1

3.6

6.9

3.8

0.3

0.4

RW2

29.8

11.6

14.6

26.0

11.8

5.1

1.0

0.0

BW3

23.0

8.7

47.3

7.5

8.3

4.3

0.6

0.3

FWP4

12.0

2.7

66.3

7.6

7.0

4.1

0.1

0.5

DW5

20.0

18.8

21.0

10.0

25.0

4.0

1.0

GP6

12.1

16.4

6.9

11.9

49.5

3.2

0.0

PW7

28.1

1.8

23.5

37.6

5.7

2.9

0.3

0.1

CP8

4.0

38.7

6.2

23.2

21.7

6.2

0.3

0.1

UHCC prairie

15.7

14.1

20.1

4.4

20.0

20.7

1.6

3.2

HD Baccharis

34.0

19.3

3.9

0.3

9.7

31.8

0.5

LD Baccharis

17.8

39.7

1.9

0.0

11.6

23.4

1.0

4.7

Sapium

9.0

0.5

6.3

3.3

55.8

9.8

1.0

14.3

Discussion

Consistent with the enemies release hypothesis, Sapium woodlands in
southeastern Texas supported communities depauperate in herbivores and
specialists, and were instead composed primarily of predators and
detritivores (Table 1, Table 3). These data support earlier predictions
of fewer herbivores and a differing arthropod community structure on
Sapium compared to native habitats. The differences in arthropod
abundance and species richness between Sapium woodlands and native
habitats were substantial (Figure 1 , Table 3). Nevertheless, Sapium may
be in the early stages of acquiring a more typical insect assemblage.
Other work has shown that introduced plants may take up to 300 years
to support an insect fauna indistinguishable from native plants (Strong
1974; Strong et al. 1984). Therefore the difference in the fauna
documented on Sapium might be consistent with only 100 years of
colonization time in Texas.

A large proportion of the species or morphospecies were infrequently
encountered on Sapium , suggesting either a high number of transient
individuals or rare individuals. This is considered typical in arthropod
communities (Siemann et al. 1999).

The differences in arthropod communities between Sapium woodlands
and native habitats might reflect unusual taxonomic, phenological,

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THE TEXAS JOURNAL OF SCIENCE— VOL. 56(4), 2004

Dimension 1

Figure 1 . Non-metric multi dimensional scaling ordination of the relative abundance of the
seven major insect orders (see Table 4) sampled from Sapium, UHCC coastal prairie
(McFadden 1978), high and low densities of Baccharis (Birch 1975), and the eight native
habitats from Cameron & Byrant (1999). Refer to methods for site abbreviations.

biochemical, and morphological properties of the exotic species (Strong
et al. 1984). Taxonomically, there are no other native tree species
belonging to the Euphorbiaceace family, although there are a number of
herbs such as Euphorbia bicolor (snow-on-the-prairie) and Croton
capitatus (woolly croton). However, phenologically and morphological¬
ly it is similar to the native mid-sized, broad-leaved deciduous trees,
such as Celtis laevigata (Bush & Van Auken 1986; Bruce et al. 1997),
suggesting that Sapium is not unusual in this regard. Sapium' s ability
to form dense monospecific stands and reduce habitat complexity in the

HARTLEY ET AL.

379

understory is unprecedented in this region, thus simple plant architecture
and or low local plant diversity might account for reduced arthropod
diversity and abundance.

Of all the native habitats examined, the grazed pasture site was most
similar in arthropod composition to Sapium woodlands (Figure 1, Table
4). Both Sapium and grazed pasture are unnatural types of habitat.
Originally the Sapium sampling location would have been coastal tail-
grass prairie approximately 100 years ago, although 90 hectares of
coastal prairie has now been restored. The UHCC coastal prairie site
(McFadden 1978) was the second most similar native site, while the
coastal prairie (Cameron & Byrant 1999) was the fourth most similar.
Sapium woodlands may have recruited some arthropods from adjacent
prairie habitat, and this may account for some degree of similarity
between the arthropod community composition of Sapium and native
coastal prairie sites sampled by McFadden (1978) and Cameron &
Bryant (1999).

Comparisons to Birch (1975), McFadden (1978), and Cameron &
Byrant (1999) are informative. However, there are differences between
the approaches that should be noted (also see methods). First, sampling
was conducted at different times and years. Birch (1975), McFadden
(1978), and Cameron & Byrant (1999) all sampled in the mid to late
1970’s, although there have been no significant, sudden, or large scale
changes (such as land use change) in the UHCC vicinity. Furthermore
Cameron & Byrant (1999) only sampled in the spring. Generally, insect
communities increase in abundance at the beginning of the growing
season and decrease at the end of the growing season, yet many popula¬
tions display substantial fluctuations. Sapium arthropod data (total
abundance and species richness) exhibited no significant pattern of
variation among the sampling periods. Secondly, sampling efforts could
differ, but are difficult to quantify or compare. Thirdly, Birch (1975)
also used a D-vac in addition to a sweep net (see Siemann 1998).
Although there are differences in approaches, the overall relative results
should not be greatly influenced by them, especially considering that
both McFadden (1978) and Cameron & Byrant (1999) state they col¬
lected 85% of the diversity, which is comparable with the Sapium data
(77-84%). This would suggest that their results are representative of the
communities they sampled. Finally, the authors determined trophic data
for McFadden (1978) from an appendix of the most common 95 species
and morphospecies (from a total of 535). It was assumed that the

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THE TEXAS JOURNAL OF SCIENCE— VOL. 56(4), 2004

complete data would have been driven by the most abundant species and
morphospecies and so the trophic data determined would reflect this.
These factors may have influenced the contrast between the insects found
on Sapium and in native habitats, but the data indicate a paucity of
herbivores found on Sapium.

In conclusion, Sapium woodlands seem to presently support an
atypical arthropod fauna, with Diptera (flies), Acari (mites) and
Araneida (spiders) as the dominant orders. Sapium' s fauna is mostly
composed of predators and detritivores with very few herbivores. The
apparent relative lack of a herbivorous food chain supports the predic¬
tion and may have important implications in ecosystem functioning.
Although Sapium woodlands in southeastern Texas appear to have
acquired few herbivores in the 100 years it has been present, it is
expected that arthropod diversity and possibly abundance will continue
to increase on Sapium and the composition of associated arthropod fauna
will change to be more similar to native communities over time. Per¬
haps the accumulation of a more robust herbivore fauna will limit
Sapium' s success as an invader in the future.

Acknowledgments

The authors would like to thank: University of Houston for access,
EPA (R82-8903), NSF (DEB-9981654) and a Wray Todd fellowship (for
MKH) for support; John Jackman, John Oswald, Ed Riley, and Jim
Woolley from the Texas A & M University Entomology department and
William Mackay at the University of Texas at El Paso, for help with
identifications; Glenn Aumann, Ann Awantang, Tim Becker, Brad
Butterfield, Candy Donahue, Will Gordon, James Hammer, Paul
Harcombe, Stephanie Hsia, June Keay, Viki Keener, Rick Lankau,
Mary Mackay, Daniel Mee, Summer Nijjer, Rachel Tardif, and Liz
Urban for assistance; Paul Harcombe, Guy Cameron and an anonymous
reviewer for helpful comments.

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MKH at: mariak@rice.edu

TEXAS J. SCI. 56(4):383-394

NOVEMBER, 2004

DIEL ACTIVITY PATTERNS OF
THE LOUISIANA PINE SNAKE {PITUOPHIS RUTHVENI)

IN EASTERN TEXAS

Marc J. Ealy, Robert R. Fleet and
D. Craig Rudolph

Texas Parks and Wildlife Department, 1700 7th St., Rm. 101
Bay City, Texas 77414;

Department of Mathematics and Statistics, Stephen F. Austin State University
Nacogdoches , Texas 75962 and
USD A Forest Service, Southern Research Station, 506 Hay ter St.

Nacogdoches, Texas 75965

Abstract.— This study examined the diel activity patterns of six Louisiana pine snakes in
eastern Texas using radio-telemetry. Snakes were monitored for 44 days on two study areas
from May to October 1996. Louisiana pine snakes were primarily diurnal with moderate
crepuscular activity, spending the night within pocket gopher burrows or inactive on the
surface. During daylight hours, snakes spent approximately 59% of their time underground
within gopher burrows, burned out/ rotten stumps, or nine-banded armadillo (. Dasypus
novemcinctus ) burrows. Remaining time was spent on the surface either close to subter¬
ranean refuge, or in long distance movements that generally terminated at another pocket
gopher burrow system. Long distance movements occurred on 45% of the days snakes were
monitored and averaged 163 m/movement. When snakes were active, movements related
to ambientair temperature; 82% of these movements occurred between 1000 and 1800 hours.
These results confirm that Louisiana pine snakes are diurnal and closely associated with
Baird’s pocket gophers and their burrow systems, and have provided new insight on the
ecology of this rare snake.

The Louisiana pine snake ( Pituophis ruthveni), first described by Stull
(1929), is a large-bodied constrictor of the family Colubridae and until
recently was considered one of 15 subspecies of Pituophis melanoleucus
(see Sweet & Parker 1990; Collins 1991; Crother et al. 2003). The
Louisiana pine snake is allopatric to other Pituophis and its distribution
is primarily restricted to the longleaf pine ( Pinus palustris ) ecosystem of
west-central Louisiana and eastern Texas (Conant 1956; Reichling
1995). The longleaf pine ecosystem is perpetuated by frequent fire
(Platt et al. 1988; Frost 1993). Louisiana pine snakes are semi-fossorial
and are closely associated with Baird’s pocket gopher ( Geomys
breviceps ) burrow systems (Rudolph & Burgdorf 1997). Baird’s pocket
gophers are the predominant prey of Louisiana pine snakes and their
burrow systems are used for foraging, shelter, escape from frequent
fires, and hibernation (Rudolph et al. 1998; 2003).

Many have reported on the apparent rarity of P. ruthveni ; this can be

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THE TEXAS JOURNAL OF SCIENCE-VOL. 56(4), 2004

partly attributed to its semi-fossorial habits and secretive nature (Conant
1956; Young & Vandeventer 1988; Rudolph & Burgdorf 1997). Only
57 records of P. ruthveni were available through 1990 (Conant 1956;
Jennings & Fritts 1983; Young & Vandeventer 1988; Reichling 1989).
As a result, this species is considered to be one of the rarest snakes in
North America (Thomas et al. 1991). Extreme rarity has prevented
researchers from collecting substantial ecological and natural history data
on the species and accounts for the paucity of available literature.

In 1993, the USD A Forest Service Southern Research Station initiated
a long term study of home range and habitat use of free ranging
Louisiana pine snakes in eastern Texas and west-central Louisiana
through the use of radio- telemetry. This portion of the study was con¬
ducted from May through October 1996 to elucidate diel activity patterns
of this snake in eastern Texas.

Study Areas

Two areas were used to monitor Louisiana pine snakes in eastern
Texas. Foxhunter’s Hill is a 500 ha longleaf pine savanna located on
the Sabine National Forest approximately 25.5 km south of Hemphill,
Texas, in Sabine County. The second area, Scrappin’ Valley, owned by
Temple-Inland Forest Products Corporation, is approximately 29 km
south of Hemphill, Texas, in Newton County. The portion of Scrappin’
Valley used as the study area is a 450 ha longleaf pine savanna.
Characteristics common to both sites are: soils with high sand content;
diverse herbaceous flora dominated by little bluestem ( Schizachyrium
scoparium) and bracken fern ( Pteridium aquilinum ); over story domi¬
nated by longleaf pine ( Pinus palustris ), sparsely distributed blackjack
oak ( Quercus marilandica) and blue jack oak ( Quercus incana ); and
areas of encroachment by sweet gum ( Liquidambar styraciflua ), sassa¬
fras ( Sassafras albidum ), and yaupon (Ilex vomitoria) as a result of past
fire suppression. Foxhunter’s Hill possesses moderate topographic
relief, average basal area of 9 m2/ha, and heavy leaf litter accumulation
and was burned by prescription in late winter of 1993. Scrappin’ Valley
has lower topographic relief than Foxhunter’s Hill, average basal area
of 6 m2/ha, moderate leaf litter accumulation, and was burned in late
winter of 1995. Generally, Scrappin’ Valley was burned annually while
Foxhunter’s Hill was burned every 3-5 years, resulting in differential
leaf litter accumulation in the two areas.

EALY, FLEET & RUDOLPH

385

Materials and Methods

Transmitter implantation.— Louisiana pine snakes were captured on
the study areas by hand or in drift fence/funnel traps. Temperature
sensitive transmitters (Holohil Systems Ltd., SI-2T) 29mm long and 10
mm in diameter with 28 cm whip antennae were implanted subcutane¬
ously following the general procedure of Weatherhead & Anderka
(1984). Transmitter life-span was approximately 18 months and maxi¬
mum transmission range was approximately 1200 m.

Radio-telemetry /data collection.— Snakes were located early in the
morning before they became active and emerged from subterranean
shelter. A Trimble GPS Professional unit and data logger was used to
record each snake’s location. Air temperature at the snake’s location
was measured with a mercury thermometer 0.5 m above the ground in
the shade. Substrate temperature was recorded in one of two ways: if
the snake was aboveground, the thermometer was placed on the substrate
as close as possible to the snake without disturbing it; if below ground,
the thermometer was inserted approximately 5 cm into the soil. Snake
body temperature was determined by comparison of transmitter pulse
rate with a calibration curve for each transmitter.

Throughout the day until sunset, transmitter pulse counts and air
temperatures were recorded at 30-45 minute intervals. When the pulse
count of a transmitter changed by becoming much slower or faster,
indicating a temperature change of the implanted transmitter, the snake
was relocated to determine if snake activity had occurred. Six snakes,
three on Foxhunter’s Hill, and three on Scrappin’ Valley were monitored
from dawn to dusk for a total of 44 snake days. Movements were
recorded and calculated only if an individual moved more than 10 m
from its previous location on a given day (Slip & Shine 1988). Move¬
ments on six additional days were recorded during the course of other
data collection and were also available. Movement distances were
calculated through the use of Trimble GPS Pathfinder Office software
(Trimble Mapping and GIS Systems Division, Sunnyvale, CA).

Periodic night checks were conducted by locating snakes at sunset and
again at midnight and before sunrise to determine if the snakes were
active nocturnally. Additional data regarding movement and choice of
underground refugia were collected from these and other snakes in
addition to the 44 snake monitoring days.

Habitat measurements were taken at each snake relocation point as
required for various aspects of research on P. ruthveni. Additional

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THE TEXAS JOURNAL OF SCIENCE— VOL. 56(4), 2004

habitat measurements were taken at 100 stratified random points deter¬
mined by overlaying a grid on the overall study site and using the inter¬
sections of the grid lines as the random points. The only habitat
measurement relevant to this study was the number of burrows counted
within an 11.2 m radius (0.04 ha) of each habitat point. Geomys
breviceps “burrows” were counted as the number of visible push-up
mounds and all other burrows were enumerated by the number of actual
openings at or near the soil surface.

Data analysis— Distance moved per snake each day was tested by a
Mann-Whitney U-test. Chi-square contingency tests were used to
evaluate the time each snake utilized above ground and below ground
environments, movement frequency, and refuge/shelter types used.
Frequency of movements during 12 two-hour time periods were evalu¬
ated by Chi-square contingency tests and all statistical analyses were
performed at an alpha level of 0.05.

Results

Six P. ruthveni (5 F, 1 M) were monitored during all or most of a
total of 44 snake days between July and October, 1996. During the 44
snake days of monitoring, individual snakes were located at the surface
between sunrise and sunset for 145 hrs of a total of 354 hrs (41 %). The
remainder of their time was spent underground in G. breviceps burrows,
nine-banded armadillo burrows, and decayed or burned stump holes and
associated root channels.

In order to determine nocturnal behavior, the six P. ruthveni were
monitored at approximately sunset, midnight, and sunrise for a total of
20 snake days during July and August. With one exception, all snakes
were located below ground in G. breviceps burrows each night ( n =
17). The exception, a female, was located on the surface beneath dense
herbaceous vegetation at sunset on three separate days and remained in
that location until the next morning. One of these instances was during
pre-ecdysis. For the 44 snake days when extensive monitoring oc¬
curred, snakes were assumed to have spent the previous night in G .
breviceps burrows, based on early morning detections, a total of 29
times. These same snakes were assumed to have spent the succeeding
night in subterranean retreats in 38 instances (35 in G. breviceps
burrows, three in D. novemcintus burrows) based on detections at dusk.
Data are not available for the remaining 21 nights.

EALY, FLEET & RUDOLPH

387

Time of Day

Figure 1. Body temperature (open circles), air temperature (open squares), and substrate
temperature (open triangles) for a Louisiana pine snake ( Pituophis ruthveni ) spending
daylight hours underground in a Baird’s pocket gopher ( Geomys breviceps ) burrow.
Adult female 143 on 14 July 1996.

Pituophis ruthveni monitored for daily activity during this study
evinced three general daily activity patterns. In 17 cases, snakes re¬
mained in G. breviceps burrow systems for the entire daily tracking
period (Fig. 1). All six snakes except one female from Scrappin’ Valley
spent at least one entire day in a G. breviceps burrow. Conversely,
three individuals spent an entire day on the surface. Two of these
individuals moved significant distances (225 m and 59 m), and the third
was in pre-ecdysis condition with clouded eyes.

In 24 cases various combinations of time were spent on the surface
and below ground. These cases were usually associated with substantial
surface movement (19 of 24), usually culminating with entrance into
another underground refuge (22 of 24) (Fig. 2). Of these 24 snake
days, 12 involved snakes that were on the surface when first located in
the morning and 12 were in G. breviceps burrow systems from which
they subsequently emerged. It is unclear if the snakes initially located
on the surface had emerged from underground refugia early or had spent
the night on the surface, although sampling for nocturnal activity sug¬
gests the former in most instances.

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THE TEXAS JOURNAL OF SCIENCE-VOL. 56(4), 2004

Figure 2. Body temperature (open circles), air temperature (open squares), and substrate
temperature (open triangles) for a Louisiana pine snake ( Pituophis ruthveni ) spending
portions of a day underground in a Baird’s pocket gopher ( Geomys breviceps) burrow and
portions above ground. Adult female 118 on 03 August 1996.

On the 27 snake days in which at least a portion of the day was spent
on the surface plus six additional snake days for which movement
distances are available, seven snakes remained in the same location,
exhibiting only minor movements of < 10 m throughout the day. One
individual moved 72 m from its initial location, but returned to its initial
location by dusk. In 25 instances snakes moved substantial distances
(> 10 m) during the day and were located an average of 163 m (range
1 1-625 m) from their initial location. Movements occurred from shortly
after sunrise until dusk with the majority (82%) between 10:00 and
18:00 hours (Fig. 3). Overall, snakes moved a substantial distance on
20 of 44 days monitored (45.5%). There was a significant difference
in frequency of movement between Scrappin’ Valley and Foxhunter’s
Hill snakes (%2 = 9.99, df — 1, P < 0.005) with the Scrappin’ Valley
snakes moving more frequently (Table 1). Daily movement distances
were calculated by summing straight line measurements between con¬
secutive locations and should be interpreted as an underestimation since
snakes rarely travel in a straight line (Secor 1994). On days when
movement occurred, snakes at Scrappin’ Valley (Table 1) moved greater
distances, (jc = 189 m, n = 19) than did those on Foxhunter’s Hill ( x

EALY, FLEET & RUDOLPH

389

Time of Day

Figure 3. Frequency distribution (%) of movements by six Louisiana pine snakes ( Pituophis
ruthveni) relative to time of day. Data for 12 May - 27 October 1996.

= 91 m, n = 7); this difference was significant (U = 40.5, df = 26,
P < 0.05).

Pine snake use of underground refugia was recorded on 44 days
during which daily activity patterns were monitored and on other days
when snakes were located for home range computation. Snakes used G.
breviceps burrows (80.9%), decayed or burned stumps (15.4%), or D.
novemcintus burrows (3.7%) as underground refugia. Based on habitat
data collected at random points (Table 2), Scrappin’ Valley had signifi¬
cantly higher densities of G. breviceps burrows (x2 = 193.9, df = 1, P
< 0.005) and other types of retreats (x2 = 10.2, df = 1, P < 0.005)
than Foxhunter’s Hill. Compared to snakes at Foxhunter’s Hill, snakes
at Scrappin’ Valley used underground retreats other than pocket gopher
burrows more frequently (x2 = 29.31, df = 1, P < 0.001).

The percent of time an individual utilized underground environments
on days snakes were monitored was determined through visual observa¬
tions and making inferences from temperature relationships based on the
snakes’ body temperature compared to air and substrate temperatures.
Snakes at Scrappin’ Valley (Table 1) spent a significantly lower propor¬
tion of daylight hours underground (45%) compared to snakes at Fox¬
hunter’s Hill (74%) (x2 =19.96, df= 1, P<0.05).

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THE TEXAS JOURNAL OF SCIENCE-VOL. 56(4), 2004

Table 1. Distance moved, movement frequency, and time spent below ground {% time
sunrise to sunset) for six Louisiana pine snakes ( Pituophis ruthveni) at Scrappin’ Valley
and Foxhunter’s Hill in eastern Texas.

Study Area

Range of
movement
(m)

Mean distance
moved per day
(m)

Movement

frequency

(%)

% Time
below
ground

Scrappin Valley

12-625

189 + 35

Foxhunter’s Hill

11-184

91+22

Combined

11-625

163+32

Table 2. Indices of burrow abundance at snake relocation points and random points (0.04
ha plot) (Scrappin’ Valley and Foxhunter’s Hill in eastern Texas).

Study Area

No. of gopher

No. of burrows

burrows at

at snake

at random

snake

relocation points

random points

relocation

points

Scrappin Valley

7.74

2.52

1.28

0.70

Foxhunter’s Hill

8.08

0.64

0.62

0.37

During the May through October period when P. ruthveni tempera¬
tures were monitored, subterranean retreats, primarily G. breviceps
burrows, provided a refuge from extreme temperatures. Pituophis
ruthveni emerged from subterranean retreats at body temperatures
ranging from 19 to 29 °C. The lower temperatures were recorded in
May and October, and the higher temperatures were presumably associ¬
ated with snakes that were re-emerging within a day or had undergone
a period of basking at the burrow entrance prior to actual emergence.
Body temperatures of snakes in subterranean retreats were generally
within 2°C of soil temperatures at a depth of 5 cm which ranged be¬
tween 20.75 and 32.5 °C.

Body temperatures of snakes present on the surface ranged from 20
to 36.75 °C. However, snakes frequently maintained body temperatures
between 25.5 and 34.5 °C by basking, even when air temperatures were
as low as 22 °C. Air temperatures never exceeded 35.5 °C during moni¬
toring periods, but P. ruthveni frequently moved into subterranean re¬
treats as air temperatures approached 35 °C.

Discussion

Surface activity of P. ruthveni was determined to be essentially
diurnal. Individuals were typically located in subterranean retreats,

EALY, FLEET & RUDOLPH

391

generally those of G. breviceps, at night. Snakes located above ground
at night were inactive and sheltered under low vegetation. Diurnally, P.
ruthveni were located above ground 41% of the time, and all recorded
movements occurred during daytime. Diurnal activity is typical of
Pituophis sp. with the exception of populations located in desert environ¬
ments where diurnal activity is severely limited by high temperatures
(Gibbons & Semlitsch 1987). Pituophis ruthveni also spent a substantial
portion of daylight hours underground (59%), generally in burrows of
G. breviceps. The close association of P. ruthveni with G. breviceps
burrows provides substantial opportunity to avoid extreme air tempera¬
tures.

The close association with the burrows of G. breviceps is consistent
with other observations of the ecology of P. ruthveni. Geornys breviceps
is the primary prey of P. ruthveni (Rudolph et al. 2003), and decline or
loss of G. breviceps populations, generally resulting from alteration of
the fire regime, is hypothesized to be an important cause of population
declines (Rudolph & Burgdorf 1997). In addition, G. breviceps burrows
are the only documented hibernaculum sites, and are used for escape
from predators and fire (Rudolph et al. 1998).

Pituophis ruthveni were relatively immobile (i.e., moved < 10 m) on
54.5% of days monitored. This is consistent with a figure of 43% for
northern pine snakes, P. melanoleucus melanoleucus , in New Jersey
(Burger & Zappalorti 1989). Relative inactivity has been hypothesized
to be a critical component of the thermal ecology of reptiles (Gans &
Dawson 1976). This may be the case with P. ruthveni because remain¬
ing immobile near a subterranean retreat provides immediate access to
two divergent thermal regimes. Huey (1982) also suggested that
inactivity conserves energy and reduces the risk of predation. In a
generally more mobile and active species, Coluber constrictor , Plummer
& Congdon (1994) found that 90% of inactivity was associated with
ecdysis. In P. ruthveni , only 13% of inactive days were associated with
ecdysis, suggesting that the previously mentioned factors may be
involved in the relative inactivity of this species.

Pituophis ruthveni moved an average of 1 63 m/d on those days when
substantial movements were undertaken. This is similar to the findings
of Fitch & Shirer (1971) for P. catenifer in Kansas (142 m/d) and
considerably greater than Parker & Brown (1980) found for P. catenifer
deserticola in Utah (71 m/d). Long-distance movements in P. ruthveni

392

THE TEXAS JOURNAL OF SCIENCE-VOL. 56(4), 2004

generally involved movement from one G. breviceps burrow system to
another and consequently reflect the dispersed distribution of these
burrow systems.

Pituophis ruthveni , during this and associated studies were found to
move very little while underground in G. breviceps burrows, typically
remaining near the point of entrance in the relatively shallow foraging
tunnels. This suggests that P. ruthveni behave as sit- and- wait predators
when hunting pocket gophers, rather than actively searching within the
burrow system. Geomys breviceps maintain an intricate burrow complex
that can reach 180 m in length (Schmidly 1983), and they can rapidly
construct an earthen plug effectively limiting movement by P. ruthveni
(Rudolph et al. 2003). These observations suggest that a sit- and- wait
strategy combined with a brief pursuit may be the most effective strategy
to capture G. breviceps.

Pituophis ruthveni behavior differed significantly, based on three
criteria, between the Scrappin’ Valley and Foxhunter’s Hill study sites.
Snakes at Scrappin’ Valley moved more frequently, moved greater
distances, and spent less time underground compared to snakes at
Foxhunter’s Hill. The Scrappin’ Valley site was also characterized by
a greater density of both G. breviceps burrows and other types of
retreats compared to the Foxhunter’s Hill site. It is possible that the
greater availability of subterranean retreats at Scrappin’ Valley resulted
in fewer restrictions on above ground activity by P. ruthveni. The
greater availability of G. breviceps burrows and other subterranean
retreats (primarily burned stump and root channels) is presumably
related to the more frequent prescribed fire regime at the Scrappin’
Valley site.

The use of subterranean retreats during the active period of the year
provided P . ruthveni with predictable escape from excessively high air
temperatures. Conversely, snakes also had direct access to basking
opportunities on the surface that allowed the snakes to maintain a higher
body temperature during substantial periods. This general pattern is
similar to the results of Himes et al. (2002) for this species in northern
Louisiana.

The diel activity budget of P. ruthveni reveals a species that is diurnal
and semifossorial as is generally typical of other members of the genus
in the United States (Fitch & Shirer 1971 ; Parker & Brown 1980; Sweet
& Parker 1990). The importance of burrows of Baird’s pocket gophers
when combined with previous data and observations (Rudolph &

EALY, FLEET & RUDOLPH

393

Burgdorf 1997; Rudolph et al. 1998; 2003) supports the hypothesis that
P. ruthveni is dependent on G. breviceps and ultimately on a frequent
fire regime that maintains the herbaceous vegetation that supports G .
breviceps populations.

Acknowledgments

B. Autrey, S. J. Burgdorf, R. R. Schaefer, R. N. Conner, R. Maxey,
and C. M. Duran provided assistance in collection of field data and
other aspects of this research. Temple-Inland Forest Products Corp.
provided access to the Scrappin’ Valley study site. The U.S. Fish and
Wildlife Service and Texas Parks and Wildlife Department provided
partial funding under Section 6 of the U. S. Endangered Species Act and
Texas Parks and Wildlife Department issued the required permits.

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Reichling, S. B. 1995. The taxonomic status of the Louisiana pine snake ( Pituophis
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Rudolph, D. C., S. J. Burgdorf, R. N. Conner, C. S. Collins, D. Saenz, R. R. Schaefer,
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MJE at: ealy@wcnet.net

TEXAS J. SCI. 56(4): 395-404

NOVEMBER, 2004

ARBOREAL BEHAVIOR IN THE TIMBER RATTLESNAKE,
CROTALUS HORRIDUS , IN EASTERN TEXAS

D. Craig Rudolph, R. R. Schaefer, D. Saenz
and R. N. Conner

Southern Research Station, JJSD A Forest Service
506 Hay ter Street, Nacogdoches, Texas 75965

Abstract.— There have been several recent reports, and anecdotal observations extending
back at least to J. J. Audubon, suggesting that the timber rattlesnake ( Crotalus horridus) is
one of the most arboreal members of the genus. Most previous records are of snakes located
at heights of less than 5 m. Telemetry studies in eastern Texas have documented more
frequent arboreal activity (16.1% of locations of sub-adult snakes) and at greater heights (up
to 14.5 m) than previously reported. Unlike previous reports, observations of arboreal
activity were restricted to sub-adult snakes (<90 cm SVL), possibly because adult snakes
in the current study area are considerably larger than those in other areas where arboreal
activity has been documented. Increasing body size and mass may preclude arboreal
behavior in larger individuals of this species. Despite considerable speculation on the
motivation(s) for arboreal activity in this species, the factors involved remain unclear.

Arboreal behavior in snakes is increasingly recognized as an
important aspect of snake ecology (Lilly white & Henderson 1993).
Anecdotal accounts of arboreal activity by timber rattlesnakes ( Crotalus
horridus) date back at least to Audubon (Klauber 1972). In a well
known painting by Audubon a timber rattlesnake is depicted attacking
Northern Mockingbirds ( Mimas polyglottos) in a shrub. This painting
has elicited considerable discussion concerning the arboreal proclivities
of timber rattlesnakes (Klauber 1972).

In recent years, increasing use of radio-telemetry to investigate the
biology of timber rattlesnakes has resulted in a proliferation of reports
and citations of arboreal activity (Saenz et al. 1996; Coupe 2001; Fogel
et al. 2002, Sealy 2002, Bartz & Sajdak 2004). During an ongoing
study of C. horridus in eastern Texas, Saenz et al. (1996) reported
several observations of arboreal behavior. Observations subsequent to
the Saenz et al. (1996) report suggest that arboreal behavior, at least by
sub-adult individuals, is more frequent in eastern Texas and involves
greater heights than previously reported.

A detailed understanding of arboreal behavior in C. horridus is
limited by the paucity of published records. Saenz et al. (1996)
suggested that increasing snake size may limit arboreal behavior in C.
horridus . Other authors have suggested that arboreal behavior may be

396

THE TEXAS JOURNAL OF SCIENCE— VOL. 56(4), 2004

related to basking, avoiding flood waters, ecdysis and foraging (Klauber
1972; Coupe 2001; Fogel et al. 2002, Sajdak & Bartz 2004), and that
females may exhibit more frequent arboreal activity than males (Coupe
2001). Additional observations reported here will help to clarify aspects
of the arboreal behavior of C. horridus.

Study Area and Methods

The study area was on and adjacent to the floodplain of the Angelina
River in Nacogdoches Co. , Texas. Specific study sites were the Stephen
F. Austin Experimental Forest located 12 km SW of Nacogdoches (31°
30’N, 94° 47’ W), and the Loco Bayou Hunt Club located 15 km WSW
of Nacogdoches (31° 31’N, 94° 50’W). Habitat at both sites consisted
of bottomland hardwood forest dominated by oaks ( Quercus sp.),
sweetgum ( Liquidamber styraciflua) and hickories {Cary a sp.); and
adjacent upland forest dominated by loblolly and shortleaf pines {Pinus
taeda and P. echinata ), oaks {Quercus sp.) and a diverse array of other
species. Portions of the bottomland habitats were subject to winter and
spring flooding in most years.

Crotalus horridus were captured as encountered during the course of
the study, transported to the laboratory, and implanted with S1-2T
transmitters (Holohil Systems Ltd.). Transmitters were implanted
subcutaneously following the general procedures of Reinert & Cundall
(1982) and Weatherhead & Anderka (1984). Snakes were retained in
the laboratory, with access to a heating pad, for approximately 7 d
following surgery to facilitate healing. Transmitters were replaced at
approximately 18 mo intervals.

Following release, snakes were relocated at irregular intervals, GPS
locations recorded, and a series of habitat measurements and other data
recorded as required for ongoing studies. In instances where individuals
were located in arboreal situations, snake height, plant species, diameter
at breast height (dbh) of supporting tree, presence of vines and other
pertinent observations were noted.

A series of climbing trials using C. horridus were conducted on
selected trees. Lengths of muscadine grape {Vitis rotundifolia) vines 3-6
cm in diameter were occasionally attached to tree trunks to simulate
situations noted during climbing events. Observation of subsequent
climbing behavior provided some indication of the arboreal abilities of
C. horridus.

A series of feeding trials were also conducted using Brown-headed

RUDOLPH ET AL.

397

Cowbirds ( Molothrus ater) . Cowbirds were captured in mist nets or box
traps, placed in cages with individual C. horridus of various sizes, and
the snakes’ subsequent behavior recorded.

Results

Thirty four C. horridus (60-140 cm SVL) were radio- tracked between
1993 and 2000 yielding more than 500 relocations. During this period
12 sub-adult snakes <90 cm SVL and with a mass <510 g were
relocated a total of 218 times. Eight of these 12 snakes were located in
arboreal situations a total of 35 times (Table 1). Each of the four snakes
<90 cm SVL never found in an arboreal location were individuals
represented by less than 10 relocation points. Snakes larger than 90 cm
SVL, range 90-140 cm, were never observed in arboreal situations, with
one exception. An adult male (136 cm SVL) was located in a shrub at
heights ranging from 0.5 to 1.2 m on three occasions during a 15 day
period. This individual had uncharacteristically occupied a hibernacu-
lum in a bottomland hardwood site prone to flooding. In each arboreal
observation the snake had been forced out of the hibernaculum and into
the shrub by rising water. This observation is not included in the
analyses that follow.

The 35 instances of arboreal behavior represent 16.1% (35 of 218) of
total observations of snakes <90 cm SVL and 17.9% (35 of 196) of
observations of those individuals located in arboreal situations at least
once. Arboreal behavior was observed in all months from March to
October, the general activity period of C. horridus in eastern Texas. Of
the minimum of 21 separate climbing events, females were involved in
11, males in 10. Contingency table comparison of arboreal relocations
vs. total relocations for females (18 of 147, 12.2%) and males (17 of
71, 23.9%) showed a slight, but significant bias favoring males (x2 =
3.88. P < 0.05).

The heights at which C. horridus were located ranged from 0.8 -
14.5 m with a mean of 5.9 m based on the 23 distinct arboreal locations
represented. Individual snakes were relocated in the same tree (n = 9),
occasionally with minor movements (n = 2) , during subsequent reloca¬
tions ranging from three to 24 days. There is no way of knowing
whether these individuals returned to the ground between observations.
Instances where snakes were relocated in the same arboreal location on
subsequent days were typically those located at greater heights, however
the irregularity of the relocation schedule makes detailed comparisons
difficult. In all cases where visual evaluation was possible, snakes were

Table 1. Snake measurements and arboreal behavior data for timber rattlesnakes ( Crotalus horridus) in eastern Texas.

398

THE TEXAS JOURNAL OF SCIENCE— VOL. 56(4), 2004

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Four observations between 5 May and 14 May 1999.
Five observations between 1 Mar. and 8 Apr. 1997.

RUDOLPH ET AL.

399

coiled or variously extended along branches or in forks of trunks or
major limbs. No instances were observed where snakes were coiled
around supporting limbs or assumed specific postures to maintain
stability in arboreal situations.

The arboreal situations occupied by C. horridus varied considerably.
Of the minimum 21 distinct climbing events observed, six were situa¬
tions where snakes were in vine tangles, dead tops of fallen trees, and
small saplings or shrubs at heights of 2.6 m or less. In the remaining
15 instances, the snakes were located in substantial trees (9.5 - 48 cm
DBH) at heights >2.5 m, often much greater. Vines, smaller diameter
trees with low branches, loose bark and leaning trunks potentially
facilitated the climbing in six of these instances. However, in the
remaining nine instances the snakes were located in canopy or sub¬
canopy trees (14 - 48 cm DBH) at heights of 4.5 - 14.5 m without
obvious characteristics that would facilitate climbing. In the most
extreme case, a C. horridus was located at a height of 14.5 m at the first
major fork of a laurel oak ( Quercus p hellos). The trunk was vertical,
with a clear bole, and no vines to facilitate climbing. Access to this site
was limited to climbing the vertical trunk or via the canopies of adjacent
trees.

Climbing trials with C. horridus <90 cm SVL demonstrated limited
climbing ability compared to other species ( Elaphe sp., Masticophis
flagellum ) that typically exhibit arboreal behavior. In cases where
smaller branches were available C. horridus were able to maneuver
slowly along horizontal or inclined branches, bridge between branches,
and coil around branches to maintain a stable hold. However, it was not
possible to elicit climbing of vertical, or nearly vertical, branches of any
diameter, or boles of trees. Throughout these trials snakes gave the
impression of awkwardness and hesitancy.

Eighteen laboratory trials were conducted in which birds ( Molothrus
ater) were presented to C. horridus of various sizes (range 75 - 104 cm
SVL), and subsequent prey capture occurred. In all instances following
the initial strike, the snakes maintained a hold on the bird until death of
the bird. Time until apparent death of the cowbirds ranged from 54-364
sec with a mean of 188 sec. Feathers appeared to present a substantial
impediment to fang penetration, and in several instances the snakes were
observed to manipulate the cowbird between their jaws without releasing
the bird, often for several min, until they were able to penetrate the
feathers with a fang. Smaller snakes that did not immediately achieve
an effective bite often had the anterior portion of their body moved

400

THE TEXAS JOURNAL OF SCIENCE— VOL. 56(4), 2004

around the cage by the struggles of the cowbirds. The overall behavior
of the snakes striking birds was distinctly different from observations of
these same snakes preying on a variety of mammalian species where
prey was struck and immediately released.

Discussion

Previously published accounts (Saenz et al. 1996; Coupe 2001; Fogel
et al. 2002) and included references and communications, Sealy 2002;
Sajdak & Bartz 2004; Bartz & Sajdak 2004) suggest that C. horridus
consistently exhibits arboreal behavior and vindicates portions of
Audubon’s early observations. However, much remains to be learned
about arboreal behavior in C. horridus , including prevalence, onto¬
genetic variation, geographic variation and motivation.

Size appears to limit arboreal behavior in C. horridus . Published
accounts (Saenz et al. 1996; Coupe 2001; Fogel et al. 2002; Sajdak &
Bartz 2004; Bartz & Sajdak 2994; this study) report only five individuals
>90 cm SVL demonstrating arboreal behavior: two individuals (99.5
and 112.5 cm SVL) reported by Coupe (2001) without specific details,
two individuals (100.5 and 98.0 cm SVL) reported by Bartz & Sajdak
(2004) engaged in courtship approximately 1 m above the ground, and
the adult male individual reported in this study at modest heights after
being forced from its hibernaculum by rising water. The relationship
between size and arboreal behavior has not been reported previously,
with the exception of Saenz et al. (1996) preliminary report of this
study, presumably due to the relatively small adult size of the more
northern populations involved in most previous reports.

This study documents more extensive arboreal behavior by C.
horridus , at least sub-adults, than previously reported (Coupe 2001;
Fogel et al. 2002; Sajdak & Bartz 2004; Bartz & Sajdak 2004). Al¬
though Klauber (1972) characterized C. horridus as “among the more
persistent climbers,” arboreal behavior has been described as uncommon
(Fogel et al. 2002), and characterized as frequent, rare, numerous
instances, rarely observed (communications in Coupe 2001) without
specific details. Only Coupe (2001) provides more specific data, stating
that C. horridus were observed in arboreal situations during 13.2% of
relocations; however, this figure is based on the subset of individuals
observed in such situations at least once. In this study sub- adults were
located in arboreal situations during 16.1% of relocations, and restricting
the data to only those individuals observed in arboreal situations at least
once (comparable to Coupe’s 2001 data) raises this figure to 17.9%.

RUDOLPH ET AL.

401

Obviously, these data are not directly comparable, primarily because C.
horridus in the more northern populations rarely reach body lengths at
which arboreal behavior becomes extremely rare in eastern Texas.

This study, including the preliminary observations reported by Saenz
et al. (1996), is the first to report arboreal activity at substantial heights.
Most previous reports are of individuals located at modest heights of 3
m or less, with a maximum of 5 m (Coupe 2001; Fogel et al. 2002;
Sajdak & Bartz 2004). In eastern Texas the mean height of arboreal
locations was 5.9 m with a maximum of 14.5 m, considerably higher
than previously reported for this species. Sub- adult C. horridus were
regularly located in the lower portions of tree canopies.

Arboreal behavior in C. horridus in eastern Texas appears to be more
frequent and involve greater heights than is the case in more northern
populations. It is important to realize, however, that this comparison is
based on sub-adult individuals in eastern Texas, individuals comparable
in size to most adults in more northern populations. These comparisons
suggest that arboreal behavior is more prevalent in the more southern
portions of the range of C. horridus. Additional data from a wider
geographic range would be desirable.

Coupe (2001) suggested that arboreal behavior might be more
prevalent among females. In eastern Texas, males were more frequently
observed in arboreal situations based on percent of observations. Over¬
all, currently available data do not demonstrate a consistent difference
in arboreal behavior between females and males.

The motivation leading to arboreal behavior in C. horridus has
elicited considerable speculation but little insight. Of the 23 individuals
involved in a minimum of 41 separate climbs and observed on a total of
107 separate days reported in Coupe (2001), Fogel et al. (2002), Sealy
(2002), Sajdak & Bartz (2004), Bartz & Sajdak (2004), and this study,
two were associated with flood waters, three with ecdysis, one with
basking by a gravid female, and four (2 pairs) with courtship. All of
these observations were of individuals at heights <5 m, generally <3
m. Attaining a preferred thermal regime (basking) could conceivably be
associated with several of the above observations and unrecognized in
others. However, in Texas obvious basking behavior is rare. Individu¬
als are generally exposed on the forest floor but do not seek open areas,
track sun flecks, or show other behaviors that could be associated with
basking. Even gravid females, which typically seek heavy cover
(hollow logs, debris piles), do not need to bask given the relatively high

402

THE TEXAS JOURNAL OF SCIENCE-VOL. 56(4), 2004

average temperatures in the region. Consequently, basking and other
activities noted above can only account for a minority of the
observations, and do not appear to be involved in the observations at
more extreme heights. These considerations may not even represent the
primary motivation that led to the initial climbing activity in all cases.

Avoidance of terrestrial predators is potentially a factor leading to
arboreal behavior. If restricted to periods when active foraging is not
occurring (ecdysis, post- feeding periods after mobility is regained)
benefits might result. However, data or observations that support this
hypothesis are not available.

Arboreal foraging is a possibility mentioned by Klauber (1972), Saenz
et al. (1996), Fogel et al. (2002), and Coupe (2001). Arboreal foraging
was verified in one instance (Sajdak & Bartz 2004) when a was observed
capturing a Yellow-bellied Sapsucker ( Sphyrapicus varius) at a height of
4.5-6 m. Verification of arboreal foraging behavior is difficult because
definitive foraging postures in arboreal situations, analogous to those
described in terrestrial situations (Reinert et al. 1984), have not been
recognized. Crotalus horridus preys primarily on endotherms (Clark
2001). Consequently, potential prey available in arboreal situations in
Texas are restricted to numerous species of birds, southern flying
squirrels ( Glaucomys volans) , squirrels ( Sciurus sp.) and a limited
variety of other small mammals. In a recent compilation of the prey of
C. horridus , Clark (2001) reported that approximately 1% of recorded
prey items were birds, although a substantial number of those identified
to species were primarily terrestrial. Squirrels of the genus Sciurus, the
primary prey of adult C. horridus in eastern Texas are often abundant
in arboreal situations. However Sciurus sp. , and in many cases even G.
volans, are too large for C. horridus, of the sizes that typically climb,
to handle.

Birds would seem to be the most likely prey of C. horridus in
arboreal situations. Climbing and predation on birds has been observed
in other pitvipers. The shedao pitviper ( Gloydius shedaoensis) in China,
a relatively thick-bodied pitviper where adults average 60-70 cm SVL,
actively climbs trees and shrubs and ambushes birds primarily during
periods of avian migration (Shine et al. 2002). Striking and holding
avian prey, presumably a secondarily acquired trait in Crotalids that prey
regularly on mammals (Martins et al. 2002; Stiles et al. 2002), may
increase the efficiency of predation on birds. Striking and holding onto
avian prey was the strategy used in the report of Sajdak & Bartz (2004),
even during a minimum vertical fall of 3 m to a lower branch. Mam-

RUDOLPH ET AL.

403

malian prey that is potentially more dangerous to C. horridus is typically
released immediately after striking (Chiszar et al. 1982; Stiles et al.
2002). Strike and release would present significant difficulties in trailing
prey that could fly, even for short distances, and would presumably be
extremely difficult from arboreal situations (Martins et al. 2002).
Observations of prey taxa, that present little potential danger or are
potentially difficult to trail or handle, that various Crotalids strike and
hold include scorpions, fishes, frogs, lizards and birds (Parker & Stotz
1977; Rubio 1998; Hayes & Duvall 1991; Reiserer 2002; Stiles et al.
2002).

The limited climbing abilities of C. horridus may limit the possibilities
of arboreal foraging to smaller snakes. The apparent lack of behaviors
such as coiling around limbs for support, or specialized support postures
used by other heavy bodied arboreal species would appear to limit the
ability of C. horridus to capture and handle prey items in arboreal situa¬
tions. The report by Sajdak & Bartz (2004) of the C. horridus falling
to a lower branch during prey capture supports this view. Despite these
limitations, foraging remains the most likely general explanation for
arboreal behavior in C. horridus.

Acknowledgments

We thank J. A. Matos, L. McBrayer, R. E. Thill, B. Parresol and R.
R. Fleet for constructive comments and suggestions on an early draft of
this manuscript. S. J. Burgdorf was a primary contributor to all aspects
of this research, and J. G. Dickson was intimately involved during the
early years of this study. M. Duran, T. Trees and J. C. Tull provided
invaluable field assistance. The U. S. Fish and Wildlife Service and
Texas Parks and Wildlife Department provided the necessary permits.
We also thank J. Mast and the members of the Loco Bayou Hunt Club
for access to study sites. The mention of trade names does not
constitute endorsement by the U. S. Department of Agriculture.

Literature Cited

Bartz, A. D. & R. A. Sajdak. 2004. Crotalus horridus (timber rattlesnake). Arboreality,
courtship. Herpetol. Rev., 35:61.

Chiszar, D., C. Andren, G. Nilson, B. O’Connell, J. S. Mestas, Jr., H. M. Smith & C.
W.Radcliffe. 1982. Strike-induced chemosensory searching in old world vipers and new
world pit vipers. Anim. Learn. Behavior, 10(2): 121-125.

Clark, R. W. 2001. Diet of the timber rattlesnake, Crotalus horridus. J. Herpetol.,
36(3):494-499.

Coupe, B. 2001. Arboreal behavior in timber rattlesnakes ( Crotalus horridus ). Herpetol.

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Rev., 32(2):83-85.

Fogel, D. D., T. J. Leonard & J. D. Fawcett. 2002. Crotalus horridus horridus (Timber
Rattlesnake). Climbing. Herpetol. Rev., 33(3):212.

Hayes, W. K. & D. Duvall. 1991. A field study of prairie rattlesnake predatory strikes.
Herpetologica, 47(1):78-81.

Klauber, L. M. 1972. Rattlesnakes: Their habits, life histories, and influence on mankind.
University of California Press. Berkeley, CA. 1536 pp.

Lillywhite, H. B. & R. W. Henderson. 1993. Behavioral and functional ecology of arboreal
snakes. Pp. 1-48, in Snakes: ecology and behavior (R. A. Seigel & J. T. Collins, eds.)
McGraw Hill, Inc., New York, NY. 414 pp.

Martins, M., O., A. V. Marques & I. Sazima. 2002. Ecological and phylogenetic
correlates of feeding habits in neotropical pitvipers of the genus Bothrops. Pp. 307-328,
in Biology of the vipers (G. W. Schuett, M. Hoggren, M. E. Douglas, & H. W. Greene,
eds.) Eagle Mountain Publ. Eagle Mountain, UT. 580 pp.

Parker, S. A. & D. Stotz. 1977. An observation on foraging behavior of the Arizona
ridge-nosed rattlesnake, Crotalus willardi willardi, (Serpentes:Crotalidae). Bull.
Maryland Herpetol. Soc., 13:123.

Reinert, H. K. & D. Cundall. 1982. An improved surgical implantation method for
radio-tracking snakes. Copeia, 1 982(3) :702-705.

Reinert, H. K., D. Cundall & L. M. Bushar. 1984. Foraging behavior of the timber
rattlesnake, Crotalus horridus. Copeia, 1 984(4) :976-981.

Reiserer, R. S. 2002. Stimulus control of caudal luring and other feeding responses: a
program for research on visual perception in vipers. Pp. 361-384, in Biology of the
vipers (G. W. Schuett, M. Hoggren, M. E. Douglas, & H. W. Greene, eds.) Eagle
Mountain Publ. Eagle Mountain, UT. 580 pp.

Rubio, M. 1998. Rattlesnake, portrait of a predator. Smithsonian Institution Press.
Washington and London. 239 pp.

Sajdak, R. A. & A. W. Bartz. 2004. Crotalus horridus (timber rattlesnake). Arbo reality,
diet. Herpetol. Rev. 31(1):60-61.

Saenz, D., S. J. Burgdorf, D. C. Rudolph & C. M. Duran. 1996. Crotalus horridus
(Timber Rattlesnake). Climbing. Herpetol. Rev., 27(3): 145.

Sealy, J. B. 2002. Ecology and behavior of the timber rattlesnake ( Crotalus horridus ) in
the upper Piedmont of North Carolina: identified threats and conservation
recommendations. Pp. 561-578, in Biology of the vipers (G. W. Schuett, M. Hoggren,
M. E. Douglas, & H. W. Greene, eds.) Eagle Mountain Publ. Eagle Mountain, UT.
580 pp.

Shine, R. L., E. Z. Sun & X. Bonnet. 2002. A review of 30 years of ecological research
on the shedao pitviper, Gloydius shedaoensis. Herpetol. Nat. Hist., 9(1): 1-14.

Stiles, K., P. Stark, D. Chiszar & H. M. Smith. 2002. Strike-induced chemosensory
searching (SICS) and trail-following behavior in copperheads (. Agkistrodon contortrix ).
Pp. 413-418, in Biology of the vipers (G. W. Schuett, M. Hoggren, M. E. Douglas, &
H. W. Greene, eds.) Eagle Mountain Publ. Eagle Mountain, UT. 580 pp.

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implantation technique for snakes. J. Herpetol., 18(3):264-269.

DCR at: crudolph01@fs.fed.us

TEXAS J. SCI. 56(4):405-414

NOVEMBER, 2004

NESTING HABITAT OF EASTERN WILD TURKEYS
{MELEAGRIS GALLOPAVO SYLVESTRIS) IN EAST TEXAS

Bobby G. Eichler* and R. Montague Whiting, Jr.

Arthur Temple College of Forestry
Stephen F. Austin State University
Nacogdoches , Texas 75962
* Current address:

Texas Parks and Wildlife Department
Mount Pleasant, Texas 75455

Abstract. — Eastern wild turkeys ( Meleagris gallopavo sylvestris) captured in Iowa and
Georgia were relocated to the Pineywoods of east Texas where they were radio-marked and
released. During the 1995 and 1996 nesting seasons, nest sites of radio-marked hens were
located and characteristics of the habitat surrounding the sites and of randomly selected sites
in the same vegetation type were evaluated using paired r-tests. Of 24 nest located, 6 were
successful. Most nests were in mature pine-hardwood stands or pine regeneration areas.
Nest sites had higher densities of living and dead grasses and higher screening cover values
than did random sites {P < 0.05). Other habitat characteristics did not differ between nest
and random sites ( P > 0.05). These results suggest that herbaceous ground cover is the
most important habitat variable which hens use when selecting nest sites. Habitat character¬
istics surrounding nests located in this study were similar to those documented in other
studies in the southeast. Although nesting habitat probably is adequate in east Texas, land
managers could increase such habitat by mowing utility rights-of-way on a two to three-year
schedule, implementing a three to five-year prescribed burning regime, thinning pine stands
at or before canopy closure, retaining slash after logging operation, and delaying site
preparation in regeneration areas until after the nesting season.

In Texas, the eastern wild turkey {Meleagris gallopavo sylvestris)
originally ranged over approximately 12, 145,000 hectares in 40 counties
in the Pineywoods Ecological Region (Newman 1945). The birds
occupied river bottom and upland forest communities. During the
1800’s, Texas settlers thought eastern wild turkey populations to be
inexhaustible (Carpenter 1959). However, commercial hunting and
extensive land clearing led to declining turkey numbers throughout the
early 1900’s (Carpenter 1959). In 1941, the Texas Legislature closed
the turkey season throughout the Pineywoods, but the action came much
too late; by 1942, less than 100 native eastern wild turkeys remained in
Texas (Newman 1945).

Records indicate that wild turkey restoration efforts by the Texas
Game, Fish and Oyster Commission began in east Texas as early as
1924 (Newman 1945; Carpenter 1959). Many unsuccessful restocking
attempts were made during the next 40 to 50 years; most failed attempts

406

THE TEXAS JOURNAL OF SCIENCE-VOL. 56(4), 2004

used pen-reared eastern wild turkeys or the Rio Grande subspecies (M.
gallop avo intermedia) . However, between 1979 and 1981, wild-trapped
eastern wild turkeys were released on two east Texas sites, and
populations flourished (Swank et al. 1985). In 1987, the Texas Parks
and Wildlife Department, in cooperation with the National Wild Turkey
Federation, initiated a large-scale eastern wild turkey restoration
program in east Texas. The program used wild- trapped eastern turkeys
acquired from southeastern and mid western states. Some restockings
were successful, but others failed and populations remained low in many
areas (I. D. Burk, per. comm.).

Wild turkey populations are sustained by annual brood productivity
(Seiss et al. 1990). Thus, nesting habitat is critical to the well-being of
the species (Badyaev 1995). In order to increase wild turkey productivi¬
ty in east Texas, suitable nesting habitat needs to be identified. The
objectives of this study were to describe vegetative characteristics
surrounding nest sites of wild turkey hens and to compare these charac¬
teristics to vegetative characteristics surrounding random sites.

Methods

Four study areas in Tyler County, Texas were stocked with wild-
trapped eastern wild turkeys relocated from Iowa and Georgia during
January and February of 1994. Twelve hens and three gobblers were
released at each site; equal numbers of hens and gobblers were from
Iowa and Georgia. Prior to release the turkeys were aged, banded and
fitted with back-pack style radio transmitters. An attempt was made to
radio-locate the birds daily for the first two weeks after release. If
mortality occurred during that period, the bird was replaced. There¬
after, the birds were radio-located at least once a week, and up to three
times a week. During February 1995, eight wild turkey hens were
captured on a study area in Trinity County; the birds were aged,
banded, fitted with transmitters and released at the point of capture. In
January of 1996, an additional 15 wild- trapped hens from Iowa were
fitted with transmitters and released on that study area.

Beginning on 1 April of 1995 and 1996 hens were radio-located three
to five times per week. When a hen exhibited very localized daily
movements, it was assumed she had initiated a nest. Once a hen was
radio-located three times in the same place, it was assumed incubation
had begun, and she was radio-located daily. After approximately 10
days of incubation, the nest location was estimated using triangulation,
azimuths, and estimated observer-to-nest distances. After the hen had

EICHLER & WHITING

407

left the nest area for at least one day, an attempt was made to locate and
determine the fate of the nest; Nests were classified as successful ( >
one egg hatched) or unsuccessful (depredated or abandoned).

Macro and micro-habitat characteristics were evaluated at each nest
location. The macro-habitat variables were forest type and tree size
class. Forest type of the stand surrounding each nest was classified as
either pine, pine-hardwood, riparian or opening; openings included food
plots, rights-of-way, pastures and seedling ( < 1.4 m tall) pine planta¬
tions. Tree size classes (trees > 1.4 m tall) were based on diameter at
breast height (DBH) of dominant trees in the area surrounding the nest
site. Size classes used were sapling (< 12.7 cm DBH), pole (12.7 to
27.9 cm DBH) and sawtimber (> 27.9 cm DBH) (Stoddard & Stoddard
1987).

Chi-square tests were used to determine if nesting hens selected
macro-habitats according to availability. Habitat composition data from
a study by George (1997) were used with Chi-square tests for Tyler
County nests. In that study, macro-habitats were classified as pure pine
forests, pine-hardwood forests, riparian forests or openings. Habitat
composition data for the Trinity County study area were gathered from
the Temple-Inland Forest Products Corporation five-year plan for the
area; macro-habitats were categorized the same as the George (1997)
study.

Micro-habitat data were collected in the area immediately surrounding
the nest site. Micro-habitat characteristics measured included basal area
of pine, basal area of hardwood, total basal area, distance to nearest
man-made edge, distance to nearest natural edge, percent canopy
closures, relative screening cover of the understory and relative densities
of the ground cover.

Basal areas were measured from the center of the nest using a 10-
factor prism. Distances to nearest man-made and natural edges were
measured using a 23 -m logger’s tape. Canopy closures of the under¬
story, midstory and overstory were evaluated using a modified point-
quadrat technique (Smeins & Slack 1982). Understory was vegetation
< 2 m tall, midstory 2 to 15 m tall, and overstory vegetation > 15 m
tall. With the nest as the plot center, a 10-m transect was established in
each cardinal direction. Along each transect, five subpoints were spaced
at 2-m intervals; the first subpoint on each transect was 2 m from the
nest site. Canopy closure data were gathered at each subpoint using a
sighting tube (Whiting & Fleet 1987; Parsons 1994). At each subpoint,

408

THE TEXAS JOURNAL OF SCIENCE-VOL. 56(4), 2004

an observer looked straight up or down through the sighting tube, and
for each height class, if vegetation obstructed the crosshairs, "yes" was
recorded. From this procedure, a percent closure score could be calcu¬
lated for each canopy layer.

Under story vegetation cover was evaluated in five strata between
ground level and 1.7 m above ground level. Each of the lower four
strata were 30 cm wide; the top stratum was 50 cm wide. Screening
cover data were gathered using a vegetation profile board (VPB). The
VPB was 1.7 m tall, 8.9 cm wide and divided into five alternating red
and white colored sections which corresponded to the five strata evalu¬
ated. The board was placed at the nest center and the percent of each
section obscured was estimated from a distance of 15 m and a height of
approximately 46 cm (Nudds 1977). Scores were based on a scale of
one to five and reflected the percentage of the board which was ob¬
scured by vegetation. Scores of one, two, three, four and five, indicated
0 to 20%, 21 to 40%, 41 to 60%, 61 to 80% and 81 to 100% obscurity,
respectively. Screening cover scores were estimated from each cardinal
direction by stratum. These values were then averaged to provide
percent screening cover for each stratum.

Relative density of ground cover (i.e., living or dead vegetation) was
evaluated using a point quadrat technique. A 10-pin frame was used to
sample ground cover within 60 cm of the ground (Parsons 1994). The
pin frame measured 80 cm high and 1 10 cm long; pins were centered at
10-cm intervals along the frame. Data were gathered at five subpoints
around each nest site. For the first subpoint, the pin frame was centered
on the actual nest bowl. The remaining four subpoints were 15 m from
the nest in the cardinal directions. At each subpoint, the pins were
lowered from approximately 60 cm and each pin-to-plant hit was record¬
ed by plant category (i.e., living woody, herbaceous, grass or dead
grass). These data were used to derive an index of relative density for
each plant category. This index was simply the number of hits by
category per 10 pins (i.e., an index of 31 for living grasses would
indicate that the 10 pins made 31 contacts with living grasses). The last
hit recorded for each pin was either litter or soil. As each pin could
have only one contact with either litter or bare soil, numbers of hits
were converted to percentages. Average height of ground cover, as
bracketed by the pin frame, also was measured at each subpoint.

Immediately after micro-habitat measurements of a nest location were
completed, micro-habitat data were collected from a random location in
the same macro-habitat type (forest type and stand class). Standing at

EICHLER & WHITING

409

the nest, the observer glanced at the second hand of his wristwatch and
used the direction it was pointing as a random direction. Using a
compass, the observer then paced a distance which had been previously
taken from a random numbers table; minimum and maximum acceptable
distances were 100 m and 250 m, respectively. Data gathered at
random locations were the same as those gathered at nest locations.
Differences in micro-habitat variables between nest sites and random
sites were evaluated using paired Mests; all tests were performed at a
0.05 alpha level.

Results

At the beginning of the 1995 and 1996 nesting seasons, there were 37
and 44 hens, respectively, with active transmitters. Although eight hens
died or were lost between the 1995 and 1996 nesting seasons, 15
additional Iowa hens were released on the Trinity County site, thus
increasing the sample size by seven. During the two nesting seasons,
24 nests were located, 11 in 1995 and 13 in 1996; six nests were
successful and 18 were unsuccessful. Twelve nests were in Trinity
County, and 12 nests were in Tyler County; the six successful nests
were in Tyler County.

The majority of nests were in pine-hardwood habitat types (11) and
openings (8) (Eichler 1999:20). In both counties, there were differences
between habitat availability and habitats selected for nesting (Table 1).
In Tyler County, openings made up only 21.0% of the study area, yet
six hens (50.0%) selected this habitat type in which to nest. Converse¬
ly, only one nest was in a pine-hardwood stand and this habitat type
made up 27.2% of the study area (x2 = 23.00, 3 df, P = 0.001) (Table
1). In Trinity County, ten of 12 (83.3%) nests were in pine-hardwood
stands which comprised 55.0% of the study area. Although riparian
forests comprised 36.0% of the area, no hens nested in that habitat (x2
= 52.23, 3 df,P = 0.001).

Thirteen of the 24 nests were in sawtimber stands; 11 were in
pine-hardwood forests and two were in riparian forests. Eight nests
were in openings; of these, four were in pine seedling stands < two
years old, two in an abandoned field, one in a grazed field, and one in
the thick vegetation (i.e., rough) bordering a food plot. The remaining
three nests were in sapling and pine pole stands. Four successful nests
were in openings (all were pine seedling stands < two years old), one
in a pine sapling stand, and one in a pine pole stand.

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THE TEXAS JOURNAL OF SCIENCE— VOL. 56(4), 2004

Table 1 . Habitat availability and use of habitat types and stand classes by nesting eastern
wild turkey hens in east Texas, spring 1995 and 1996. Habitat composition differed from
utilization rates at Tyler County sites ( X 2 = 23.00, 3 df, PC0.001) and Boggy Slough
sites (X2 = 52.23, 3 df, P< 0.001).

Tyler County _ Boggy Slough

Habitat Habitat

composition Nests composition Nests All nests

Habitat

<%)

(No.)

(%>

(%)

(No.)

(%)

(No.)

(%)

Habitat type

Pure pine

30.7

25.0

4.0

00.0

12.6

Pine-hardwood

27.2

8.3

55.0

83.3

45.8

Riparian

21.1

16.7

36.0

00.0

8.3

Opening

21.0

50.0

5.0

16.7

33.3

Total

100.0

Stand class

Opening

50.0

16.7

33.3

Sapling

16.7

00.0

8.3

Pole

8.3

00.0

4.2

Sawtimber

25.0

83.3

54.2

Total

100.0

Some micro-habitat variables differed between nest sites and random
sites (Table 2). In all strata, screening cover values at nest sites were
higher than those at random sites; the differences were significant in the
0.31 to 0.60 m and the 1.21 to 1.70 m strata and approached signifi¬
cance in the 0.00 to 0.30 m stratum (Table 2) . The largest difference
was in the 0.31 to 0.60 m stratum where screening cover averaged about
14% higher at nest than at random sites. Ground cover densities were
greater at nest than at random sites for all except the herbaceous
category. Ground cover densities for both living grass and dead grass
were significantly higher at nest sites than at random locations (Table 2).
Although not statistically significant, canopy closures in the midstory
were more open at nest sites than random locations (Table 2).

Discussion

In this study, hens selected pine habitat types and openings in which
to nests. Previous studies in the Southeast have shown similar results
(Campo et al. 1989; Seiss et al. 1990; Sisson et al. 1990; Still &
Baumann 1990). In a previous east Texas study, 89% of the nests were
in upland pine forest types; however, as opposed to this study, those
nests were equally distributed among size classes of timber (Campo et
al. 1989). In South Carolina, Still & Baumann (1990) found 21 of 37
nests in pine habitats and in Georgia, Sisson et al. (1990) found 83% of
all nests in pine stands. However, in Mississippi, mature pine stands

EICHLER & WHITING

411

Table 2. Results of paired r-tests (24 df) comparing micro-habitat characteristics of eastern
wild turkey nest sites to random sites ( n = 24) in east Texas, 1995-1996.

Habitat component

Nest

sites

Random

sites

Distance from edge (m)

Natural

39.3

42.7

0.298

0.769

Manmade

40.0

35.7

0.449

0.658

Basal area (m2/ha)a

Pine

11.2

12.4

-0.834

0.413

Hardwood

5.7

5.20

-0.290

0.775

Total

17.0

17.6

-1.000

0.327

Canopy coverage (%)a

Understory ( < 2 m)

57.8

56.7

-0.249

0.805

Midstory (2-15 m)

53.9

60.8

-2.029

0.054

Overstory (> 15 m)

42.2

44.7

-1.334

0.195

Screening cover (%)

0.00 - 0.30 m

93.3

86.7

2.205

0.055

0.31 - 0.60 m

79.4

65.4

2.893

0.008

0.61 - 0.90 m

64.4

53.1

1.450

0.161

0.91 - 1.20 m

58.1

49.6

1.228

0.232

1.21 - 1.70 m

46.9

33.8

2.328

0.029

Ground cover density (hits / 10 pins)

Living grass

31.7

25.3

2.559

0.018

Dead grass

10.4

3.1

2.119

0.045

Herbaceous

6.5

6.7

-0.073

0.942

Woody species

13.2

10.9

1.239

0.228

Litter (%)

88.4

89.0

-0.187

0.854

Height of ground cover (cm)

25.8

23.5

0.965

0.354

a Only tested in sapling, pole and sawtimber stands.

contained the most nests (18 of 38) but were used according to availa¬
bility (Seiss et al. 1990). In that study, other habitats in which hens
nested included bottomland hardwoods and pine and hardwood regenera¬
tion areas.

Use of early successional habitats for nesting is also similar to
findings of other studies (Everett et al. 1981; Campo et al. 1989; Seiss
et al. 1990; Still & Baumann 1990). Seiss et al. (1990) found 36.8% of
all nests in regeneration areas whereas that type made up only 12.5% of
available habitat. In South Carolina, Still & Baumann (1990) found 10
of 37 (27%) nests in seed-tree cuts or clearcuts < 10 years old, and in
a previous east Texas study, 26% of the hens nested in pine regeneration
stands one to seven years old (Campo et al. 1989); in this study 25.0%
of hens nested in regeneration areas. Everett et al. (1981) found that
rights-of-way with roughs one to three years old were preferred nesting
habitat in Alabama.

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THE TEXAS JOURNAL OF SCIENCE— VOL. 56(4), 2004

Prescribed burning may be an important factor for nest site selection.
In Trinity County, 10 of the 12 nests were in pine uplands which were
burned on a three to five-year regime. These results are similar to those
of Sisson et al. (1990) who found that most nests (74%) were in upland
pine stands on a one to three- year burn rotation; in that study, such
stands comprised only 7.2% of the area. Conversely, in Alabama,
Exum et al. (1987) found 89% of nesting hens used areas left unburned
for three or more years.

In 1996, three of seven nests in Trinity County were in pine
sawtimber stands which had been thinned < two months prior to nesting
season. All three nests were concealed by logging slash. Previous
studies have shown that hens prefer nesting in thinned stands (Hillestad
1973; Lutz & Crawford 1987; Campo et al. 1989) and use logging slash
as concealment (Martin 1984; Lutz & Crawford 1987; Swanson 1993).
Hillestad (1973) found that four of seven hens selected recently cut-over
loblolly pine, shortleaf pine, or sweetgum stands in which to nest. In
Oregon, Lutz & Crawford (1987) found that nesting hens used thinned
conifer stands more frequently than expected (P < 0.05) and that nests
were commonly adjacent to slash.

In this study, nests sites had abundant screening cover in the 0.00 -
0.30 and 0.31 - 0.60 m strata with values ranging from 80-95%. Nests
sites in pole and sawtimber stands had lower basal area and canopy
closure values than did random sites (Eichler 1999), and higher densities
of living grasses and woody seedlings. These results parallel those of
other studies which have shown that nest sites normally have lower
densities of overstory trees, basal areas and canopy closures, and higher
screening concealment than do random locations (Lazarus & Porter
1985; Holbrook et al. 1987; Lutz & Crawford 1987; Campo et al. 1989,
Still & Baumann 1990, Swanson 1993; Lopez 1996). In the Post Oak
Savannah Region of east Texas, nest sites occurred in areas with
relatively high coverage of forbs in the understory and ground layers
(Lopez 1996). Still & Baumann (1990) found that nesting hens pre¬
ferred low to moderately stocked stands, suggesting that ground cover
was important. Holbrook et al. (1987) found that cover below the 2-m
level was more dense around nests than at random locations.

Characteristics of habitats used by nesting hens in this study were
very similar to those in other studies in the Southeast. These results
suggest that nesting habitat is adequate in east Texas (Eichler 1999).

EICHLER & WHITING

413

However, there are several practices which land managers could use to
increase nest success. This study indicated that herbaceous ground
cover is the most important habitat variable hens use when selecting nest
locations. In forested stands, a three to five-year burning regime would
seem to be appropriate to stimulate and maintain herbaceous densities for
nesting throughout the Piney woods of east Texas. Additionally, thinning
pole and sawtimber stands would allow for this same type of ground
cover. After logging operations, slash and tree tops should be left as is
to provide cover at least until after the nesting season. Likewise, in
newly created regeneration areas, site preparation practices should be
delayed until after the nesting season when possible. Lastly, utility
rights-of-way should be mowed on a two to three-year schedule; a
mosaic of two to three-year roughs would allow for nesting habitat and
discourage the growth of brush thickets.

Acknowledgments

We thank Jason Hoffman, Phillip LeWallen and Stacy Roland for
field assistance. Jim George and Jacky Chen aided with data analysis.
Thanks to John Burk (Texas Parks and Wildlife Department, Eastern
Wild Turkey Program Specialist) for his knowledge of east Texas
restocking efforts. International Paper Company and Temple-Inland
Forest Products Corporation allowed us access to their lands. This
project was funded by the National Wild Turkey Federation, Texas
Parks and Wildlife Department, and the Arthur Temple College of
Forestry at Stephen F. Austin State University.

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Arkansas Ozark Highlands. Condor, 97( 1 ) :22 1 -232.

Campo, J. J., C. R. Hopkins & W. G. Swank. 1989. Nest habitat use by eastern wild
turkeys in eastern Texas. Proc. Annu. Conf. Southeast. Assoc. Fish and Wildl.
Agencies, 43:350-354.

Carpenter, C. 1959. Return of an exile. Texas Game and Fish, 1 7( 1) :24-25 .

Eichler, B. G. 1999. Nesting and brook rearing habitat of eastern wild turkeys in east
Texas. Unpublished M.S. Thesis, Stephen F. Austin State University, Nacogdoches,
Texas, 48 pp.

Everett, D. D., D. W. Speake & W. K. Maddox. 1981. Use of rights-of-way by nesting
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Exum, J. H., J. A. McGlincy, D. W. Speake, J. L. Buckner & F. M. Stanley. 1987.
Ecology of the eastern wild turkey in an intensively managed pine forest in southern
Alabama. Tall Timbers Res. Sta. Bull. 23, Tallahassee, Florida, 70 pp.

George, J. R. 1997. Comparison of eastern wild turkey broodstock relocated into the
Pineywoods Ecological Region of Texas. Unpublished M.S. Thesis, Stephen F. Austin

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State University, Nacogdoches, Texas, 90 pp.

Hillestad, H. O. 1973. Movements, behavior, and nesting ecology of the wild turkey in
eastern Alabama. Pages 109-123, in G. C. Sanderson and H. C. Schultz, editors. Wild
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Holbrook, H. T., M. R. Vaughan & P. T. Bromley. 1987. Wild turkey habitat preference
and recruitment in intensively managed Piedmont forests. J. Wildl. Manage.,
5 1 ( 1 ) : 1 82- 1 87.

Lazarus, J. E. & W. F. Porter. 1985. Nest habitat selection by wild turkeys in Minnesota.
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Lopez, R. R. 1996. Population dynamics of eastern wild turkeys relocated into the Post
Oak Savannah of Texas. Unpublished M.S. Thesis, Texas A&M University, College
Station, Texas, 59 pp.

Lutz, R. S. & J. A. Crawford. 1987. Reproductive success and nesting habitat of
Merriam’s wild turkeys in Oregon. J. Wildl. Manage., 51(4):783-787.

Martin, D. J. 1984. The influence of selected timber management practices on habitat use
by wild turkeys in east Texas. Unpublished M.S. Thesis, Texas A&M University,
College Station, Texas, 129 pp.

Newman, C. C. 1945. Turkey restocking efforts in east Texas. J. Wildl. Manage.
9(4): 279-289.

Nudds, T. D. 1977. Quantifying the vegetative structure of wildlife cover. Wildl. Soc.
Bull. 5(3): 113-1 17.

Parsons, D. S. 1994. Nesting, brood habitat, and utilization of planted food plots by
northern bobwhite in east Texas. Unpublished M.S. Thesis, Stephen F. Austin State
University, Nacogdoches, Texas, 115 pp.

Seiss, R. S., P. S. Phalen & G. A. Hurst. 1990. Wild turkey nesting habitat and success
rates. Proc. Natl. Wild Turkey Symp., 6:18-24.

Sisson, D. C., D. W. Speake, J. L. Landers & J. L. Buchner. 1990. Effects of prescribed
burning on wild turkey habitat preference and nest site selection in south Georgia. Proc.
Natl. Wild Turkey Symp., 6:44-50.

Smeins, F. E. & R. D. Slack. 1982. Fundamentals of ecology laboratory manual. Second
edition. Kendall/Hunt Publ., Dubuque, Iowa, 140 pp.

Still, H. R., Jr. & D. P. Baumann, Jr. 1990. Wild turkey nesting ecology on the Frances
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Stoddard, C. H. & G. M. Stoddard. 1987. Essentials of forestry practice. Fourth edition.
John Wiley & Sons, New York, 432 pp.

Swank, W. G., D. J. Martin, J. J. Campo & C. R. Hopkins. 1985. Mortality and survival
of wild-trapped eastern wild turkeys in Texas. Proc. Natl. Wild Turkey Symp.,
5:113-120.

Swanson, D. A. 1993. Population dynamics of the wild turkey in West Virginia.
Unpublished Ph. D. Dissertation, West Virginia University, Morgantown, 168 pp.

Whiting, R. M. , Jr. & R. R. Fleet. 1987. Bird and small mammal communities of
loblolly-shortleaf pine stands in east Texas. Pages 49-66, in H. A. Pearson, F. E.
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Technical Report SO-68, 293 pp.

BGE at: bobby. eichler@tpwd. state. tx. us

TEXAS J. SCI. 56(4):4 15-426

NOVEMBER, 2004

THE RED-COCKADED WOODPECKER:
INTERACTIONS WITH FIRE, SNAGS, FUNGI, RAT SNAKES
AND PILEATED WOODPECKERS

Richard N. Conner, Daniel Saenz
and D. Craig Rudolph

Wildlife Habitat and Silviculture Laboratory
Southern Research Station, USD A Forest Service, 506 Hay ter St.

Nacogdoches, Texas 75965-3556

Abstract. — Red-cockaded woodpecker (Pico ides borealis ) adaptation to fire-maintained
southern pine ecosystems has involved several important interactions: (1) the reduction of
hardwood frequency in the pine ecosystem because of frequent fires, (2) the softening of pine
heartwood by red heart fungus ( Phellinus pirn) that hastens cavity excavation by the species,
(3) the woodpecker’s use of the pine’s resin system to create q barrier against rat snakes
(Elaphe sp.), and (4) the woodpecker as a keystone cavity excavator for secondary-cavity
users. Historically, frequent, low-intensity ground fires in southern pine uplands reduced
the availability of dead trees (snags) that are typically used by other woodpecker species for
cavity excavation. Behavioral adaptation has permitted red-cockaded woodpeckers to use
living pines for their cavity trees and thus exploit the frequently burned pine uplands.
Further, it is proposed that recent observations of pileated woodpecker (Dryocopus pileatus )
destruction of red-cockaded woodpecker cavities may be related to the exclusion of fire,
which has increased the number of snags and pileated woodpeckers. Red-cockaded wood¬
peckers mostly depend on red heart fungus to soften the heartwood of their cavity trees,
allowing cavity excavation to proceed more quickly. Red-cockaded woodpeckers use the
cavity tree’s resin system to create a barrier that serves as a deterrent against rat snake
predation by excavating small wounds, termed resin wells, above and below cavity entrances.
It is suggested that red-cockaded woodpeckers are a keystone species in fire-maintained
southern pine ecosystems because, historically, they were the only species that regularly
could excavate cavities in living pines within these ecosystems. Many of the more than 30
vertebrate and invertebrate species known to use red-cockaded woodpecker cavities are
highly dependent on this woodpecker in fire-maintained upland pine forests.

The red-cockaded woodpecker ( Picoides borealis ) evolved in a
landscape where frequent, low-intensity fires burned within upland
southern pine ecosystems. The fires reduced the numbers of hardwoods,
and it is suggested that they also reduced the numbers of dead trees
(snags) relative to their abundances in hardwood stands along riparian
areas and bottomlands (Conner et al. 2001a). Hardwood snags, which
serve as typical cavity trees for many woodpecker species in this
scenario, were probably scarce. It was in this landscape that the
red-cockaded woodpecker adapted to excavating cavities in live pine
trees.

The extended length of time required to excavate cavities in live pines

416

THE TEXAS JOURNAL OF SCIENCE-VOL. 56(4), 2004

and the subsequent rarity of completed cavities in this ecosystem appear
to be closely linked to the evolution of cooperative breeding in the red-
cockaded woodpecker (Walters et al. 1988; 1992; Conner & Rudolph
1995). Cavities for nesting and roosting in living pines require a long
time to excavate (Conner & Rudolph 1995; Harding & Walters 2002)
and are so rare across the pine forest landscape that it is to the advan¬
tage of young woodpeckers, particularly young males, to forego dis¬
persal and defer breeding until a breeding slot opens up in their natal
cluster of cavity trees or a nearby cavity-tree cluster (Walters et al.
1992). These young woodpeckers from previous nesting efforts remain
with the breeding pair and assist in subsequent nesting efforts by incu¬
bating eggs, feeding and brooding young, excavating cavities, and
helping to defend the group’s territory (Ligon 1970; Walters et al. 1988;
Conner et al. 2001a).

In this paper a scenario is suggested by which historically frequent,
low-intensity ground fires in southern pine uplands reduced the availa¬
bility of dead trees (snags) that are typically used by woodpeckers for
cavity excavation. Standing dead trees were more abundant in the more
mesic hardwood sites where other species of woodpeckers are abundant.
Behavioral adaptations permitted red-cockaded woodpeckers to excavate
cavities into living pines for nesting and roosting. Thus, red-cockaded
woodpeckers exploited the frequently burned pine uplands (Conner et al .
2001a), where the rarity of more typical cavity-excavation sites in dead
branches and dead trees historically excluded or decreased the abundance
of other woodpecker species in the southeastern United States because
they typically do not make cavities in live pines (Conner et al. 1975;
Kilham 1983). Discussion is also presented on how the woodpecker’s
adaptation to pine ecosystems has benefited other species by creating
cavities in a relatively cavity-barren landscape.

The Interaction of Fire
with Upland Pine Landscapes

Fossil pollen records indicate that fire-maintained pine ecosystems
began to spread from peninsular Florida approximately 12,000 years ago
and arrived at the western extreme of their distribution in Texas about
4,000 years ago (Webb 1987). This expansion was permitted by the
retreat of the Laurentide ice sheet of the Wisconsin glaciation to the
north (Conner et al. 2001a). Bartram (1791) described the original
longleaf pine ( Pinus palustris ) forests as nearly unbroken expanses of
widely spaced pines within a sea of grass. Fire, which burned in both

CONNER ET AL.

417

the winter and growing season, was an integral part of the spread of
pine ecosystems (Bonnicksen 2000; Conner et al. 2001a). Historically,
frequent fires were ignited primarily during dry periods by lightning,
Native Americans, and early settlers (Catesby 1731; Michaux 1802).
The frequent fires burned day and night and meandered across the land¬
scape until they encountered sites too isolated or too wet to burn (Frost
1993; Glitzenstein et al. 1995). The fires killed invading hardwoods in
the upland pine ecosystem and maintained the herbaceous ground cover
that consisted primarily of grasses and forbs (Jackson et al. 1986;
Glitzenstein et al. 1995). Throughout the South, fallen pine needles and
dried grasses served as fuel for the ground fires, which burned every
one to three-plus years (Landers 1991; Glitzenstein et al. 1995;
Bonnicksen 2000). Michaux’ s (1802) observations indicate that longleaf
pine forests which occupied seven- tenths of the landscape in the
Carolinas were burned annually.

Because hardwoods were rare in well-burned pine uplands (Chapman
1909; Platt et al. 1988; Frost 1993), live pines and pine snags were the
primary sources of potential nest sites for woodpeckers. Although low-
intensity ground fires may burn existing snags created by lightning and
bark beetle ( Dendroctonus sp., Ips sp.) infestation, they typically do not
generate sufficient heat to kill pines, which would create new snags
(Conner 1981; Conner et al. 2001a). Therefore, it is suggested that
even pine snags may have been scarce in southern pine ecosystems.

Interaction of Red-cockaded Woodpeckers
with Fungi

The use of living pines as sites to excavate cavities for nesting and
roosting resulted in an increase in the length of time required for the
woodpeckers to make a cavity. Most woodpecker species in eastern
North America can excavate a new cavity in a dead, decayed snag in
two to four weeks (Conner et al. 1975; 1976; Kilham 1983). Pileated
woodpeckers (. Dryocopus pileatus ) can excavate a cavity in 23 days in
the eastern United States, but excavation time can take three to six
weeks in the Pacific Northwest (Bull & Jackson 1995). Downy wood¬
peckers ( Picoides pubescens) can excavate a complete cavity in two
weeks, whereas hairy woodpeckers ( Picoides villosus ) can take up to
four weeks (Kilham 1983). Red-bellied woodpeckers ( Melanerpes
carolinus) typically can excavate a completed cavity within two weeks
(Shackelford et al. 2000) and red-headed woodpeckers ( Melanerpes
erythrocephalus) within three weeks (Jackson 1976). Cavity excavation

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THE TEXAS JOURNAL OF SCIENCE-VOL. 56(4), 2004

by northern flickers (Colap tes auratus) can take up to four weeks (Burns
1900). Lawrence (1967) observed that average cavity excavation time
for northern flickers was 12.1 days, hairy woodpeckers 19.7 days,
downy woodpeckers 16.0 days, and yellow-bellied sapsuckers
(Sphyrapicus varius) 19.7 days.

Because red-cockaded woodpeckers use living pines for cavity trees,
where the heartwood is often not decayed (Conner & Locke 1982),
cavity excavation may require numerous years (Conner & Rudolph
1995). Unlike snags, which often have decayed sapwood and heart-
wood, the sapwood of live pines is not decayed (Conner & Locke 1982),
and red-cockaded woodpeckers have to excavate through 8 to 16 cm of
solid wood (Conner et al. 1994). Increasing sapwood thickness and the
presence of flowing pine resin that seeps from the wound caused by
cavity excavation further complicates the process and slows the rate of
excavation (Conner et al. 1994; Conner & Rudolph 1995; Conner et al.
2001a). If resin flow is abundant, the woodpeckers typically must wait
for the resin to crystallize before recommencing excavation, again,
increasing the time required for cavity excavation (Conner & Rudolph
1995). Cavity excavation rates in red-cockaded woodpeckers may be
influenced by the availability of suitable cavities (Harding & Walters
2002). As the need for cavities increases within a group of wood¬
peckers, the birds may accelerate their excavation activities (Conner et
al. 2002).

Although red-cockaded woodpeckers can excavate a completed cavity
into a pine with undecayed heartwood and sapwood (Conner & Locke
1982), the presence of red heart fungal ( Phellinus pini ) decay in the
heartwood has an influence on the time required to excavate a complete
cavity (Conner & Rudolph 1995). Red-cockaded woodpeckers are able
to detect the presence of the fungus within the boles of the pines and
actively select pines with red heart fungal decay for cavity trees (Conner
& Locke 1982). Red heart fungus enters the heartwood of pines via
broken branch stubs (Conner & Locke 1982; Conner et al. 2004). After
gaining access to the heartwood of a pine, at least 15 to 20 years of
growth and decay within the heartwood are required before the fungus
produces a sporophore (conk) on the bole of the pine (Conner et al.
2004). This same 15- to 20-year time period is required for the fungus
to decay a minimally sufficient diameter of heartwood (12 cm; Conner
et al. 2004) for a woodpecker cavity. Although the age of the pine
appears to be the primary factor associated with increasing frequency of
heartwood decay (Conner et al. 1994), tree spacing and growth rate also

CONNER ET AL.

419

have an influence (Conner et al . 2004) . Older pines tend to have higher
frequencies of heartwood decay and pines growing slowly in diameter
prune lower branches more slowly and appear to have higher frequency
of heartwood decay (Conner et al. 2004). Increased time during the
natural limb pruning process allows more time for spores to infect wood
tissue.

As red heart fungus decays the heartwood it softens the wood, and
decayed heartwood is more easily excavated than sound heartwood. The
presence of decayed heartwood can decrease the time required for cavity
excavation by 1.3 years (Conner et al. 1994). Even with heartwood
decay present in many cavity trees, an average of 1.8 years in loblolly
( Pinus taeda) (n = 9 excavations), 2.4 years in shortleaf pines ( P .
echinata) (n = 12 excavations), and 6.3 years in longleaf pines (n = 12
excavations) is required to fully excavate a cavity (Conner & Rudolph
1995). Many red-cockaded woodpecker cavity trees are lost annually
to bark beetles, lightning, wind action, and enlargement by pileated
woodpeckers (Conner et al. 1991). Thus, the availability of pines
infected with red heart fungus may determine whether red-cockaded
woodpeckers have a sufficient number of useable cavity trees available
for nesting and roosting in a given year.

Interaction of Red-cockaded Woodpeckers
with Resin and Rat Snakes

Adaptation to contending with resin that flows from living pines when
cavities are excavated has affected the interaction between red-cockaded
woodpeckers and rat snakes ( Elaphe sp.) and enhanced the survival of
the woodpecker. Southern pines produce and maintain pine resin (gum)
within an elaborate system of canals and ducts that extends from the
pine’s needles down into its roots. Resin is a mixture of primarily light
resin oils (monoterpenes), which serve as solvents, and the heavier resin
acids (diterpenes) , which give the resin its viscous and sticky nature
(Hodges et al. 1977).

The resin system in pines has evolved as their primary defense against
bark beetles (Hodges et al. 1979). When bark beetles attack, the pine
flushes the wound with resin and if sufficient resin is present, the
attacking beetles are “pitched out.” A similar response occurs when
red-cockaded woodpeckers initiate cavity excavation. If resin flow is
very high, it will temporarily interfere with cavity excavation as noted
previously.

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THE TEXAS JOURNAL OF SCIENCE— VOL. 56(4), 2004

Red-cockaded woodpeckers nesting and roosting in living pines are
extremely vulnerable to predation by rat snakes (Neal et al. 1993).
Predictable, long-term use of individual cavities allows the local snake
population to learn the location of cavities (Neal et al. 1993), and living
pines with intact bark are easily climbed by rat snakes (Rudolph et al.
1990b). However, red-cockaded woodpeckers derive substantial protec¬
tion from rat snakes by taking advantage of resin produced by pines to
establish a resin barrier that prevents access to cavities by rat snakes.
As cavities approach completion, red-cockaded woodpeckers excavate
a series of small (1-2 cm) wounds into the cambium on the pine’s bole
around and above and below their cavity entrance. These wounds,
termed resin wells, are pecked daily by the woodpeckers and the repeat¬
ed pecking causes continuous wounding of the xylem-cambial boundary,
keeping a stream of clear, fresh pine resin flowing from the wells and
down the pine’s bole. Multiple resin wells on a healthy cavity tree
create a substantial barrier of sticky fresh resin that serves as a deterrent
to climbing rat snakes (Ligon 1970; Jackson 1974; Rudolph et al.
1990b). However, repeated wounding of cavity trees over several years
can decrease the ability of the pines to produce resin (Conner et al.
2001b) and pines with inadequate resin flow are abandoned by the
woodpeckers (Conner & Rudolph 1995). Red-cockaded woodpeckers
must continue to excavate new cavities to replace cavities with inade¬
quate resin barriers and cavity trees lost to mortality factors or cavity
enlargement by other woodpeckers.

Red-cockaded woodpeckers can detect how much resin a pine can
produce (Conner et al. 1998). The socially dominant breeding male
red-cockaded woodpecker selects the cavity tree that produces the most
resin for his roost cavity. It is the breeding male’s roost tree that
usually becomes the breeding pair’s nest tree. By selecting the cavity
tree with the highest resin yield, the nesting effort of the breeding pair
seems to receive the highest protection possible from rat snake predation
(Conner et al. 1998).

Red-cockaded Woodpeckers
as a Keystone Cavity Excavator

In the historic fire-maintained upland pine ecosystems of the South
where pines existed nearly as a tree monoculture (Chapman 1909; Platt
et al. 1988; Frost 1993), red-cockaded woodpeckers were the only
woodpeckers able to excavate complete cavities in living pines regularly
(Ligon 1970; Conner et al. 2001a). Reports of other North American
species of woodpecker excavating cavities in live portions of living pines

CONNER ET AL.

421

in the eastern United States are extremely rare or nonexistent (Bent
1939; Reller 1972; Conner et al. 1975; Jackson 1976; Kilham 1983).
Red-cockaded woodpeckers historically were and continue to be a
keystone species because they are the primary woodpecker species to
provide cavities for more than 30 other wildlife species within fire-
maintained pine ecosystems of the South (Table 1).

If dead trees were rare because they were consumed by the frequent
ground fires, other woodpecker species and cavities created by them
were likely also rare. Data on woodpecker species use of well-burned
open pine habitats versus mixed pine-hardwood habitats support the
argument that other woodpecker species were less abundant in the
historic fire-maintained pine forests of the South than in habitats where
hardwoods were present (Shackelford & Conner 1997). Detections of
pileated woodpeckers (mean number detected per 3.5 ha plot sector)
were 33 % higher (0.85 per plot visit versus 0.64) in infrequently burned
pine-hardwood forest habitats than in more regularly burned longleaf
pine habitats. Detections of red-bellied woodpeckers and northern
flickers were 24% higher (1.56 per plot visit versus 1.26) and 75%
higher (0.35 per plot visit versus 0.20), respectively, in pine-hardwood
versus open pine habitats. The differences in the abundance of other
Picoides were even more extreme. Detections of hairy and downy
woodpeckers were 350% higher (0.27 per plot visit versus 0.06) and
2300% higher (0.24 per plot visit versus 0.01), respectively, in
pine-hardwood versus open pine habitats. In contrast, a mean of 0.46
red-cockaded woodpeckers were detected per plot visit in the open pine
habitats whereas none was detected in the pine-hardwood habitats
(Shackelford & Conner 1997).

Support for this suggestion that red-cockaded woodpeckers likely were
and continue to be a keystone cavity provider for other cavity nesters in
well-burned, fire-maintained southern pine ecosystems comes from the
abundance of observations of other species using red-cockaded wood¬
pecker cavities. Numerous vertebrate and invertebrate species are
known to use red-cockaded woodpecker cavities (Table 1). Because so
many other cavity-nesting species are dependent on red-cockaded wood¬
peckers for cavities, forest biodiversity would suffer substantially in the
absence of this endangered woodpecker in fire-maintained pine eco¬
systems of the South. Several species, such as red-bellied and red¬
headed woodpeckers and southern flying squirrels appear to compete
actively with red-cockaded woodpeckers for intact cavities (Jackson
1978; Neal et al. 1992; Kappes & Harris 1995). The fact that red-

422

THE TEXAS JOURNAL OF SCIENCE— VOL. 56(4), 2004

Table 1. Vertebrate and invertebrate species observed using unenlarged and enlarged
red-cockaded woodpecker cavities in the southeastern United States.

Cavity occupant

References for observation

Birds

American kestrel ( Falco sparverius)
Brown-headed nuthatch (Sitta pusilla )

Carolina chickadee ( Poecile carolinensis)
Eastern bluebird ( Sialia sialis )

Eastern screech-owl ( Otus asio )

European starling (Sturnus vulgaris)

Great crested flycatcher (Myiarchus crinitus)
Northern flicker ( Colaptes auratus )

Pileated woodpecker ( Dryocopus pileatus )
Red-bellied woodpecker (Melanerpes carolinus )
Red-headed woodpecker (M. erythrocephalus )
Tufted titmouse (Baeolophus bicolor)
White-breasted nuthatch (Sitta carolinensis)
Wood duck (Aix sponsa)

(Rudolph et al. 1990a)

(Jackson 1978)

(Beckett 1971)

(Baker 1971; Jackson 1978)
(Baker 1971; Conner et al. 1997)
(Dennis 1971; Jackson 1978)
(Baker 1971; Conner et al. 1997)
(Baker 1971; Dennis 1971)
(Baker 1971; Jackson 1978)
(Dennis 1971; Jackson 1978)
(Baker 1971; Beckett 1971)
(Baker 1971; Beckett 1971)
(Baker 1971)

(Baker 1971)

Mammals

Eastern gray squirrel (Sciurus carolinensis)
Evening bat (Nycticeius humeralis)

Fox squirrel ( Sciurus niger)

Raccoon (Procyon lotor)

Southern flying squirrel (Glaucomys volans)

(Dennis 1971; Jackson 1978)
(Rudolph et al. 1990a)

(Baker 1971; Jackson 1978)
(Loeb 1993)

(Baker 1971; Beckett 1971)

Reptiles and amphibians

Broad-headed skink ( Eumeces laticeps)
Five-lined skink (Eumeces fasciatus)
Gray treefrogs (Hyla versicolor &

H. chrysoscelis)

Rat snake (Elaphe obsoleta)

(Conner et al. 1997)

(Jackson 1978)

(Jackson 1978; Conner et al. 1997)
(Baker 1971; Dennis 1971)

Arthropods

Ants

Honey bee (Apis mellifera)
Moths (Lepidoptera)

Mud daubers (Sphecidae)
Paper wasps (3 Polistes sp.)
Spiders

(Conner et al. 1997)

(Dennis 1971; Jackson 1978)
(Conner et al. 1997)

(Conner et al. 1997)

(Dennis 1971; Rudolph et al. 1990a)
(Conner et al. 1997)

headed and red-bellied woodpeckers, two woodpeckers that normally are
primary excavators, regularly use red-cockaded woodpecker cavities for
nesting over a wide geographic area (Neal et al. 1992) provides compel¬
ling evidence of the keystone role red-cockaded woodpeckers play in
upland pine ecosystems. Red-bellied woodpeckers have been reported
using red-cockaded woodpecker cavities more than any other species of
bird throughout the South.

Pileated woodpeckers enlarge the entrance to red-cockaded wood¬
pecker cavities such that they are no longer useable by the endangered
woodpecker (Carter et al. 1989). Red-cockaded woodpeckers likely do
not use these enlarged cavities because of their increased vulnerability

CONNER ET AL.

423

to predators and competitors. Once a cavity entrance is enlarged,
however, larger secondary cavity users, such as the American kestrel,
eastern screech-owl, northern flicker, fox squirrel, raccoon, and wood
duck, are able to use the cavity (Table 1).

Anthropogenic forces have greatly altered the southern forest land¬
scape over the past 150 years (Frost 1993; Conner et al. 2001a). Exclu¬
sion and suppression of fire from fire-maintained ecosystems and con¬
version of pine forests to other land uses have occurred south wide.
Such changes have permitted hardwood species to invade the previously
open pine uplands and likely increased the availability of dead trees
across the previously pine-dominated landscape. Snags do not always
ignite under modern day prescribed fire conditions, especially when
nearly all burns are conducted during winter under cool, humid condi¬
tions when the risk of wildfire is low. These changes have permitted
other species of woodpeckers to be in closer proximity to red-cockaded
woodpeckers than they were historically (Saenz et al . 2002) . A serious
consequence of this change is the high rate of damage done to red-
cockaded woodpecker cavities by pileated woodpeckers (Conner et al.
1991; Conner & Rudolph 1995; Saenz et al. 1998; 2002). The rate of
damage is so severe that many red-cockaded woodpecker populations
suffer an annual net loss of useable cavities. In Texas, red-cockaded
woodpecker populations on the Angelina National Forest averaged an
annual net loss of 4.6 useable cavities over a 10 year period (Conner et
al. 1991; Conner & Rudolph 1995). The loss of cavities to tree death
(57 cavity trees) was roughly equal to the loss due to pileated wood¬
pecker enlargement (55 cavity trees).

Red-cockaded woodpeckers could not have evolved in the fire-main¬
tained pine ecosystems of the South if they suffered such a loss rate
historically. They would have lost cavities faster than they could have
excavated them. Pileated woodpecker abundance and their current rate
of cavity destruction likely are elevated above what occurred in the
South in the historic fire-maintained pine ecosystems of pre-Columbian
times. Testing this hypotheses would be somewhat problematic in
present day landscapes. Because of the large home range of a pileated
woodpecker pair and red-cockaded woodpecker group, large tracts
(5,000+ ha) of unbroken well-burned longleaf pine forest that are not
fragmented from a timber-type and land-use perspective and still con¬
tained populations of red-cockaded woodpeckers would be needed to test
the hypotheses. Such landscape conditions are now only a historic
memory (Frost 1993; Conner et al. 2001a).

424

THE TEXAS JOURNAL OF SCIENCE-VOL. 56(4), 2004

Acknowledgments

We thank J. A. Jackson, N. E. Koerth, C. E. Shackelford, and J. R.
Walters for constructive comments on an early draft of the manuscript.
Research on the red-cockaded woodpecker was done under U.S. Fish
and Wildlife Service federal permit TE832201-0 to Richard N. Conner.

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RNC at: c_connerrn@titan . sfasu . edu

TEXAS J. SCI. 56(4): 427-440

NOVEMBER, 2004

FEEDING HABITS OF SONGBIRDS IN
EAST TEXAS CLEARCUTS DURING WINTER

Donald W. Worthington, R. Montague Whiting, Jr.
and Janies G. Dickson

Arthur Temple College of Forestry, Stephen F. Austin State University
Nacogdoches , Texas 75962 and
U. S. Forest Service, Southern Research Station
Nacogdoches, Texas 75965

Abstract.— This east Texas study was undertaken to determine the importance of seeds
of forbs, grasses, and woody shrubs to songbirds wintering in young pine plantations which
had been established utilizing the clearcut regeneration system. The feeding habits and
preferences of four species of songbirds, northern cardinals ( Cardinalis cardinalis), song
sparrows {Melospiza melodia), dark-eyed juncos {Junco hyemalis), and white-throated
sparrows ( Zonotrichia albicollis ) were examined from November to February of 1980-81,
1981-82, and 1982-83. Differences in consumption percentages were compared among bird
species using AN OVA and Duncan’s multiple range tests. Paired /-tests were used to
compare seeds consumed to seeds available by bird species. Differences ( P < 0.05) existed
among bird species in consumption percentages of seeds of various genera. Northern
cardinals selected seeds of Callicarpa, Croton, Datura , and Galactia. Song sparrows used
seeds of Ambrosia, Panicum, and Seteria in excess of abundance. Dark-eyed juncos also
selected Ambrosia as well as Eragrostis and Parietaria over seeds of other genera.
Ambrosia, Parietaria, Aristida, and Viola were preferred by white-throated sparrows.

Of the 4.7 million ha of commercial forest land in East Texas, 1.8
million are owned by forest industry (McWilliams & Lord 1988). Most
such lands are intensively managed for pine on a short rotation ( < 50
years), evenage basis. A common practice on industrial forest lands is
to clearcut the marketable timber at rotation age, prepare the site, and
plant pine seedlings. After site preparation, growth and seed production
of grasses and forbs are stimulated by decreased competition for nutri¬
ents, water, and sunlight. In the winter months, seeds of such plants are
a valuable food source for birds.

Few data exist on food habits and preferences or food availability to
free-ranging songbirds wintering in young southern pine plantations.
Therefore, the objectives of this study were to analyze winter foods of
northern cardinals ( Cardinalis cardinalis ), song sparrows ( Melospiza
melodia ), dark-eyed juncos (, Junco hyemalis ), and white-throated
sparrows {Zonotrichia albicollis) collected on areas which had been
recently clearcut, site prepared, and planted to pine seedlings, and to

428

THE TEXAS JOURNAL OF SCIENCE-VOL. 56(4), 2004

determine if these species were selecting seeds of certain genera or if
their feeding habits were dependent on seed availability.

Methods

Two study areas in the Piney woods Ecological Region of east Texas
were selected, one in Nacogdoches County and another in Angelina
County. Although the areas were in different counties, they were less
than 20 km apart. Both areas had been clearcut, then residual vegetation
sheared and along with debris, raked into long piles called windrows.
The windrows were burned on the Angelina County study area. Both
areas were planted with one-year-old pine seedlings during the study
period. With one exception, soils on both study areas were well-drained
fine sandy loams or loamy sands. A small part of the Angelina County
study area was nearly level, thus poorly drained (Worthington 1984).

Northern cardinals, dark-eyed juncos, and song sparrows were
collected on the study areas during November, December, January, and
February of 1980-81, 1981-82, and 1982-83; white-throated sparrows
were collected in 1982-83 only. Efforts were made to collect five
individuals of each species on each study area per month. All birds
were collected in the morning. Each collected bird was immediately
weighed to the nearest 0.5 grams. The digestive tract (esophagus,
proventriculus, gizzard) was then removed and injected with 1 CC of
10% formalin (Dillery 1965) to stop the digestive process. The tract
was placed in a self-sealing plastic bag along with an identification
number. The location where the bird was first observed was marked
with plastic flagging bearing the bird’s identification number. Upon
returning from the field, each digestive tract was frozen and stored.

In the laboratory, the contents of each digestive tract were dried at
38 °C for 48 hours, then weighed to the nearest 0.0001 g. Digestive
tract contents were then separated into four groups, namely plant seeds,
insect parts, grit, or unidentified material. Seeds were then separated to
genus using keys (Musil 1963; Landers & Johnson 1976) and a U.S.
Forest Service reference seed collection. Seeds not identified were kept
separate, labeled unknown, and assigned a number. Many of these
unknown seeds were later identified. All food materials were then
redried at 38 °C for 48 hours and weighed to the nearest 0.0001 g.

Seeds on the ground, presumably available to the collected birds,

WORTHINGTON, WHITING & DICKSON

429

were sampled during the 1981-82 and 1982-83 study periods, usually the
same day the birds were collected. Seeds were sampled on five 10 cm
radius subplots in the area where each bird was first observed. The first
subplot was where the bird was originally observed and the others were
in each cardinal direction, 2 m from the first subplot. Food materials
were collected using a hand-held power vacuum. Seeds on standing
vegetation directly above the subplots also were collected.

In the laboratory, availability samples were frozen for 48 hours to kill
insects, then coarse debris was removed. The remaining material was
passed through a series of sieves to sort seeds by size class and remove
fine debris. A binocular dissecting scope was used when separating
seeds from fine debris. The seeds were sorted, dried, and weighed in
the same manner as were seeds in the digestive tracts of the birds. The
five subplot samples were combined to form a single availability sample
for analyses.

For each bird species, the number of individuals that consumed each
seed genus was determined by study area. Each value was then divided
by the total number of birds of that species to obtain frequency of
occurrence. Differences in frequencies of occurrence were tested among
bird species by study area using two-by-four Chi-square tests.

Due to differences in body weights and total digestive tract content
weights among the four bird species (Worthington 1984:61), actual
weights of seed genera consumed were not compared among the bird
species. Instead, weights of all identified and unidentified seeds in each
bird’s digestive tract were summed and the weight of each genus was
converted to a percent of that sum. These values reflected consumption
percentages and were compared among the four bird species. Seeds
available to the birds were evaluated similarly. The conversion of actual
weights to percentages also allowed for comparisons between consumed
and available seeds. Insect parts, grit, and unidentified material were
not compared.

Differences among bird species in seed consumption percentages were
tested using ANOVA with Duncan’s multiple range tests. Differences in
seed availability percentages were tested in the same manner. For each
genus, paired t- tests were used to compare percentages of seeds
consumed to percentages of seeds available by bird species and study

430

THE TEXAS JOURNAL OF SCIENCE-VOL. 56(4), 2004

area. As seed availability data were not collected in 1980-81, seed
consumption data from that year were not used when comparing seeds
consumed to those available.

In order for a seed genus to be included in the statistical comparisons
of digestive tracts, it had to average at least 2% of consumed seeds, by
weight, for at least one bird species. To be included in comparisons of
availability data, a genus had to comprise at least 4% of the available
seeds, by weight, for at least one bird species. Throughout the study,
the null hypothesis used was that of no difference among groups being
tested. The rejection level was set at 0.05 for all tests.

Results

Ninety-five northern cardinals, 59 song sparrows, and 86 dark-eyed
juncos were collected during the three winters; 45 white- throated
sparrows were collected in the winter of 1982-83. Unidentified material
comprised 64.2 , 67.0, 65.7, and 72.9% of weights of digestive tract
contents of northern cardinals, song sparrows, dark-eyed juncos, and
white- throated sparrows, respectively; identifiable seeds made up 23.5,
16.5, 18.2, and 14.3% of digestive tract content weights of the four
species, respectively. With one exception, small amounts of greenery,
insects, and grit made up the remainder; one northern cardinal had con¬
sumed a ground skink (Scincella lateralis). Most unidentified material
was in the gizzard. It was assumed that proportions of unidentifiable
material in that organ were the same as those identifiable (West 1973).

Seeds consumed Seeds of 38 genera were identified and recorded
in digestive tracts of the birds (Worthington 1984:64-74). Eight groups
of seeds could not be identified, but only one was consumed in greater
than trace (i.e., < 1.0%) quantities. With one exception, seeds of all
identifiable genera recorded in digestive tracts were also recorded in
availability samples; no Datura seeds were recorded in availability
samples.

In Nacogdoches County, differences existed among bird species in
frequencies of occurrence of seeds of 10 genera (Table 1). A higher
proportion of the northern cardinal digestive tracts contained seeds of
Callicarpa, Croton, and Datura than did those of the other three bird
species. Conversely, Ambrosia occurred in a lower proportion of
northern cardinals than in the other three species. Eragrostis and

WORTHINGTON, WHITING & DICKSON

431

Table 1 . Numbers of birds and frequency of occurrence of seeds in digestive tracts of
northern cardinals (NOCA), song sparrows (SOSP), dark-eyed juncos (DEJU), and
white-throated sparrows (WTSP, 1982-1983 only) collected in eastern Texas during
winter 1980-81, 1981-82, and 1982-83. Within a row, a different letter indicates
different frequencies of occurrence among bird species at the 0.05 level.

Seed

genera

NOCA

n %

SOSP

n %

DEJU

n %

WTSP

n %

Nacogdoches County

Amaranthus

12.3a

18.2a

51.1b

23.8a

<0.001

Ambrosia

7.0a

45.5b

55.3b

71.4b

<0.001

Callicarpa

40.4a

9.1b

0.0b

9.5b

<0.001

Carex

7.0

9.1

0.0

0.153

Croton

49.1a

0.0b

4.8b

<0.001

Cyperus

3.5a

27.3b

17.0b

0.0a

0.008

Datura

50.1a

18.2b

6.4b

0.0b

<0.001

Digitaria

21.1

36.4

27.7

4.8

0.120

Eragrostis

0.0a

45.5c

25.5b

0.0a

<0.001

Panicum

3.5a

54.6c

23.4b

0.0a

<0.001

Parietaria

0.0a

9.1a

42.6b

57.1b

<0.001

Paspalum

7.0

18.2

4.3

0.0

<0.201

Phytolacca

35.1a

18.2ab

6.4b

0.0b

<0.001

Rudbeckia

0.0

4.3

0.0

<0.284

Sample size

Angelina County

Amaranthus

0.0a

4.2a

30.8b

4.5a

<0.001

Ambrosia

10.5a

31.3b

43.6b

50.0b

0.003

Callicarpa

36.8a

0.0b

<00001

Carex

31.6a

33.3a

2.6b

16.7b

0.002

Croton

34.2a

2.1b

2.6b

0.0b

<0.001

Cyperus

2.6a

16.7ab

25.6b

25.0b

0.031

Datura

39.5a

6.3b

0.0b

<0.001

Digitaria

0.0a

14.6b

18.0b

4.5ab

0.029

Eragrostis

0.0

6.3

10.3

4.5

0.252

Panicum

2.6a

79.2b

79.5b

33.3c

<0.001

Parietaria

0.0

2.1

2.6

0.0

0.693

Paspalum

5.3a

4.2a

20.5b

0.0a

0.008

Phytolacca

0.0

8.3

5.1

0.0

0.172

Rudbeckia

0.0a

2.1a

25.6b

0.0a

<0.001

Sample size

432

THE TEXAS JOURNAL OF SCIENCE— VOL. 56(4), 2004

Panicum seeds were found in greater proportions of song sparrow
digestive tracts than in those of the other three species and in more
dark-eyed junco tracts than in northern cardinal or white- throated
sparrow tracts. Amaranthus occurred in a higher proportion of dark¬
eyed juncos than in the other three bird species. A majority of white-
throated sparrows consumed Ambrosia and Parietaria.

In Angelina County, Callicarpa, Croton , and Datura were recorded
in higher proportions of northern cardinal digestive tracts than in those
of the other three species (Table 1). Conversely, Ambrosia and
Panicum were found in lower proportions of northern cardinal digestive
tracts than in digestive tracts of the other species. Ambrosia was found
in half of white- throated sparrows, and Panicum occurred in almost 80%
of the song sparrows and dark- eyed juncos. Finally, higher proportions
of dark-eyed juncos than the other species consumed Amaranthus ,
Paspalum, and Rudbeckia.

Seeds of 23 genera comprised at least 2% of the total weight of seeds
in the digestive tracts of one or more bird species (Worthington
1 984: 64-74) . Percent consumption of 1 2 of these genera differed among
bird species (Table 2). Combined, Croton and Datura comprised
approximately 64 and 43 % of the weight of seeds in the digestive tracts
of northern cardinals collected on the Nacogdoches County and Angelina
County study areas, respectively. On both study areas, these combined
percentages were higher than those of the other three bird species (Table
2). Song sparrows and dark-eyed juncos consumed relatively large
quantities of Ambrosia , Digitaria , and Panicum on both study areas.
Percent consumption of these genera by song sparrows and dark-eyed
juncos were generally higher than for northern cardinals and white-
throated sparrows, except for Ambrosia which made up a higher per¬
centage of the digestive tract contents of white-throated sparrows than
of the other species (Table 2). On the Nacogdoches County study area,
white-throated sparrows also consumed relatively more Parietaria than
did the other species.

Seeds available. — Eighty-two genera of seeds were collected on the
two study areas, 72 on the Nacogdoches County study area and 61 on
the Angelina County study area (Worthington 1984:62-63). Fifty-one
genera were common to both areas; 21 and 10 were exclusive to
Nacogdoches County and Angelina County, respectively. However,

WORTHINGTON, WHITING & DICKSON

433

Table 2. Weights (in percent) of seeds recorded in digestive tracts of northern cardinals
(NOCA), song sparrows (SOSP), dark-eyed juncos (DEJU), and white-throated sparrows
(WTSP, 1982-1983 only) collected in eastern Texas during winter 1980-81, 1981-82, and
1982-83. Only genera for which there were significant differences among bird species
are shown. Within a row by study area, a different letter denotes different proportions
among bird species at the 0.05 level.

Nacogdoches County Angelina County

Seed genera

NOCA

SOSP

DEJU

WTSP

NOCA

SOSP

DEJU

WTSP

Amaranthus

0.39a

2.07ab 26.46c

13.30b

0.00a

1.43a

10.50b

3.72ab

Ambrosia

0.35a

24.94b

26.42b

49.05c

4.18a

11.64a

9.98a

39.41b

Callicarpa

8.08a

4.55ab

0.00b

1.99b

17.21a

0.00b

Carex

1.28

0.79

0.00

5.58ab

10.18b

1.87a

4.48ab

Croton

34.40a

0.00b

2.94b

21.00a

1.50a

0.93b

0.00b

Datura

30.04a

2.29b

0.65b

0.00b

22.50a

0.44b

0.00b

Digitaria

0.30a

15.24b

8.12b

1.14a

0.00a

0.92ab

3.31b

0.80ab

Eragrostis

0.00a

7.01b

5.50b

0.00a

0.00

1.25

0.74

0.11

Panicum

0.07a

6.50b

3.84b

0.00a

0.27a

42.74b

34.81b

13.91a

Parietaria

0.00a

8.54ab

15.34b

28.05c

0.00

1.35

0.55

0.00

Paspalum

1.99

6.79

1.91

0.00

0.25a

1.07a

7.10b

0.00a

Phytolacca

11.53a

10.67a

1.53b

0.00b

0.00

3.28

1.40

0.00

Total (%)

88.44

89.39

89.77

96.47

71.26

75.80

71.19

62.43

Sample size

0.55

0.00

only 16 genera each contributed a minimum of 4% of the seeds available
to at least one bird species.

The genera of frequently occurring seeds included Andropogon,
Digitaria, Panicum, Phytolacca , Rhus, Solidago, and Uniola. On the
Nacogdoches County study area, there were differences among bird
species in seed availability frequencies of five commonly occurring
genera (Worthington 1984:34). However, only Ambrosia, Digitaria,
and Eragrostis comprised at least 2% of the weight of seeds consumed.
Ambrosia occurred more frequently in white-throated sparrow and song
sparrow food availability samples than in those of northern cardinals,
and Digitaria was recorded in higher percentages of song sparrow and
dark-eyed junco than white- throated sparrow food availability samples.
Eragrostis was found in a higher percentage of song sparrow food
availability samples than in those of the other species (Worthington
1984:34). For the Angelina County study area, frequencies of only two
seed genera differed among food availability samples (Worthington
1984:35). Neither of these, Eupatorium and Heterotheca , could be
considered important food items to the collected birds.

434

THE TEXAS JOURNAL OF SCIENCE- VOL. 56(4), 2004

Table 3. Weights (in percent) of seeds available to northern cardinals (NOCA), song
sparrows (SOSP), dark-eyed juncos (DEJU), and white-throated sparrows (WTSP,
1982-1983 only) collected in eastern Texas during winter 1981-82 and 1982-83. Genera
shown are those for which there were differences in percent availability and/or percent
consumption. Within a row by study area, a different letter denotes different proportions
at the 0.05 level.

Nacogdoches County Angelina County

Seed genera

NOCA

SOSP

DEJU

WTSP

NOCA

SOSP

DEJU

WTSP

Amaranthus

8.78a

4.54a

25.92c

17.28b

0.56

3.11

3.40

1.64

Ambrosia

0.89

3.13

4.36

3.51

0.14a

5.79ab

8.25b

1.31ab

Callicarpa

7.68

6.21

3.74

1.81

2.30

0.10

0.00

0.79

Car ex

0.02

0.00

0.03

0.00

0.09

4.27

0.47

3.32

Croton

4.95

0.49

4.74

1.65

0.30

0.02

0.24

0.51

Digitaria

1.13a

14.23b

3.41a

0.31a

0.00a

0.34a

1.96b

0.49a

Eragrostis

0.15

0.75

0.26

0.00

1.09

0.71

0.13

3.08

Eupatorium

1.69

3.25

0.52

2.06

2.33

7.90

1.88

3.89

Galactia

0.28a

5.94b

1.25a

0.65a

0.00

0.17

0.00

Heterotheca

0.95

5.01

1.28

3.18

7.72

2.29

6.96

12.83

Panicum

5.18

7.74

2.63

0.44

10.54a

25.99b

26.00b

1 1 .02a

Parietaria

0.00

0.21

0.10

0.35

0.00

Paspalum

0.74

0.93

0.06

0.17

1.57

0.92

0.00

1.28

Phytolacca

14.16a

5.33a

10.30a

30.11b

1.13

2.17

2.43

0.18

Rhus

29.26

33.77

21.88

28.93

21.75a

5.14b

15.94ab

24.42a

Uniola

0.43

0.00

0.63

0.64

7.28

9.42

9.56

8.26

Sample size

There were some differences in weights (in percent) of seeds available
to the bird species in each county (Table 3). In Nacogdoches County,
there were differences among species for Amaranthus, Digitaria,
Galactia, and Phytolacca. There was a higher proportion of Amaran¬
thus seeds in dark-eyed junco availability samples than in those of the
other species, and a higher proportion in white-throated sparrow samples
than in northern cardinal or song sparrow samples. Song sparrow
availability samples contained higher proportions of Digitaria and
Galactia seeds than did samples for the other species, and Phytolacca
seeds ranked higher in white-throated sparrow samples than in samples
for the other species (Table 3).

In Angelina County, there were differences in seed availability
percentages of Ambrosia , Digitaria , Panicum , and Rhus among bird
species. Both Ambrosia and Panicum seeds were less available to
northern cardinals than to the other species. Digitaria seeds ranked
higher for dark- eyed juncos than for the other species, but made up less

WORTHINGTON, WHITING & DICKSON

435

than 2% of the food available to that species. Rhus, which comprised
large proportions of the seeds available on both study areas (Table 3),
was not an important food source to any species.

Seeds selected.— Callicarpa, Croton, Datura, Galactia, and
Phytolacca comprised 90% of the seeds consumed by northern cardinals
in Nacogdoches County during the winters of 1981-82 and 1982-83
(Table 4); Croton, Datura, and Galactia were consumed in excess of
availability. The same was true of Callicarpa and Croton in Angelina
County. Phytolacca availability exceeded consumption in Nacogdoches
County but was not recorded in any Angelina County digestive tracts
(Table 4).

Only seven song sparrows were collected in Nacogdoches County,
thus statistical comparisons are weak at best. However, almost 35% of
the seeds identified in the digestive tracts of those birds were Ambrosia.
Seeds of that genus, Care) c, Panicum, and Seteria were dominant in
Angelina County song sparrows. Consumption percentages of the two
latter genera were greater than availability percentages (Table 4).

For darked-eyed juncos from Nacogdoches County, consumption of
Ambrosia, Eragrostis, and Parietaria exceeded availability. Amaran-
thus, which was readily available on that study area, comprised slightly
over 25% of the seeds consumed. In Angelina County, seeds of
Amaranthus, Ambrosia, Digitaria, and Panicum comprised almost 70%
of identifiable seeds in dark-eyed junco digestive tracts; consumption and
availability percentages of these genera were similar (Table 4).

White-throated sparrows were collected only in 1982-83. In both
counties, Ambrosia compromised the largest proportion of identifiable
seeds. Consumption of that genus and Parietaria exceeded availability
in Nacogdoches County. In Angelina County, Ambrosia, Aristida, and
Viola demonstrated similar trends. Amaranthus in Nacogdoches County
and Cy perns and Panicum in Angelina County were important food
items for which consumption and availability percentages did not differ
(Table 4). Rhus seeds were recorded in two white- throated sparrows in
Angelina County.

Discussion

Although identifiable seeds comprised relatively small proportions of
digestive tracts, this study provided strong evidence that northern
cardinals, song sparrows, dark-eyed juncos, and white-throated sparrows

436

THE TEXAS JOURNAL OF SCIENCE-VOL. 56(4), 2004

Table 4. Comparisons of percent seed availability and percent seed consumption for
northern cardinals, song sparrows, dark-eyed juncos, and white-throated sparrows in
eastern Texas during winter 1981-82 and 1982-83. Paired /-tests values also are shown.

Nacogdoches County Angelina County

Seed genera

Pet.

Avail.

Pet.

Cons

P -
value

Pet.

Avail.

Pet.

Cons.

P-

value

Northern cardinals

n = 42

n = 29

Amaranthus

8.78

0.19

0.006

0.57

0.00

0.194

Callicarpa

7.68

9.22

0.481

2.63

19.09

0.030

Carex

0.02

1.91

0.230

1.03

6.36

0.162

Croton

4.95

46.01

<0.001

0.31

26.81

0.001

Datura

0.00

24.35

<0.001

0.00

6.66

0.113

Galactia

0.28

5.16

0.041

0.00

1.000

Heterotheca

0.95

0.01

0.049

7.69

0.00

0.047

Myrica

2.17

0.00

0.274

5.16

0.00

0.153

Panicum

5.18

0.03

0.018

10.77

0.33

0.024

Phytolacca

14.16

5.31

0.016

1.15

0.00

0.179

Rhus

29.26

0.00

<0.001

22.92

0.00

0.002

Uniola

0.43

0.00

0.310

7.91

3.66

0.381

Song sparrows

n = 1

n = 39

Amaranthus

4.54

0.87

0.252

3.11

1.77

0.615

Ambrosia

3.28

34.91

0.053

5.79

11.41

0.227

Carex

0.00

1.23

0.356

4.27

8.47

0.265

Digitaria

14.23

19.29

0.734

0.34

0.49

0.880

Eupatorium

3.25

0.00

0.352

7.90

0.00

0.001

Panicum

7.74

2.15

0.343

25.99

44.48

0.010

Phytolacca

5.33

0.00

0.120

2.17

2.60

0.894

Rhus

33.74

0.00

0.071

5.14

0.00

0.042

Seteria

0.00

1.000

0.00

6.35

0.044

Uniola

0.00

1.000

9.42

0.03

0.004

Dark-eyed juncos

n — 37

n = 24

Amaranthus

26.10

25.63

0.912

3.40

11.27

0.110

Ambrosia

4.33

29.60

<0.001

8.25

13.88

0.454

Digitaria

3.37

5.93

0.337

1.96

5.25

0.312

Eragrostis

0.27

5.62

0.044

0.13

1.12

0.169

Heterotheca

1.29

0.00

0:049

6.96

0.00

0.035

Panicum

2.63

3.37

0.641

25.95

39.23

0.166

Parietaria

0.10

19.49

<0.001

0.00

0.89

0.094

Phytolacca

10.20

0.30

<0.001

2.43

2.28

0.658

Rhus

21.75

0.00

<0.001

15.91

0.00

0.025

Uniola

0.63

2.28

0.135

9.54

2.22

0.117

White-throated

sparrows*

n — 21

n — 24

Amaranthus

17.28

13.30

0.645

1.64

3.72

0.637

Ambrosia

3.51

49.05

<0.001

1.31

39.41

0.001

Aristida

0.00

1.000

0.00

11.99

0.041

Cyperus

0.13

0.00

0.892

3.20

8.88

0.409

Eupatorium

2.06

0.00

0.134

3.89

0.00

0.106

Heterotheca

3.18

0.14

0.181

12.83

0.00

0.016

Panicum

0.44

0.00

0.014

11.02

13.91

0.948

Parietaria

0.35

28.05

0.002

0.00

1.000

Phytolacca

30.11

0.00

<0.001

0.18

0.00

0.319

Rhus

28.93

0.00

0.001

24.42

1.28

0.008

Uniola

0.64

0.00

0.329

8.26

0.40

0.057

Viola

0.00

2.35

0.126

0.00

6.28

0.020

* Collected in winter 1982-83 only.

WORTHINGTON, WHITING & DICKSON

437

selected seeds of some genera over those of others. Korschgen (1980)
noted that if a food item occurred in high numbers of individuals and in
high volume within the individuals, the food was of high quality or
preference. In this study, three or four genera met these criteria for
each bird species. For most of these genera, consumption exceeded
availability.

Seeds utilized by northern cardinals were very different from those
used by the other species. With study areas combined, Callicarpa,
Croton , and Datura comprised approximately 69 % of the seeds identi¬
fied in northern cardinal digestive tracts. These genera made up only
trace proportions in digestive tracts of the other bird species. The
importance of Croton and Callicarpa to northern cardinals is well-
documented (Martin et al. 1951 ; Halkin & Linville 1999). Carex, Rhus ,
Setaria , and Panicum have also been classified as important to northern
cardinals (Halkin & Linville 1999). Although seeds of these genera
were collected on the study areas, they made up minor portions of
northern cardinal diets, and no Rhus was recorded in any northern
cardinal. No mention of northern cardinals consuming Datura was
found in the literature. Reasons for the absence of Datura seeds in
availability samples are unknown; Datura plants were present on both
study areas.

Although there were similarities in diets of song sparrows, dark-eyed
juncos, and white-throated sparrows, the relative rank of the important
genera varied among species. For song sparrows, Panicum made up
38% of identifiable seeds; Ambrosia (15%) ranked second and Carex
(7%) third. Neither Martin et al. (1951) nor Arcese et al. (2002) listed
Panicum as an important food source for song sparrows. Results of this
study contradict those findings, and it is possible that the low number of
song sparrows collected in Nacogdoches County was due to the lack of
Panicum. Ambrosia seeds are an important winter food item for song
sparrows (Martin et al. 1951), as are those of Amaranthus, Digitaria ,
and Setaria (Arcese et al. 2002). In this study, seeds of these three
genera comprised relatively minor proportions of song sparrows diets.

In dark-eyed junco digestive tracts, Ambrosia (23%), Amaranthus
(20%), Panicum (18%), and Parietaria (12%) made up almost three-
fourths of the identifiable seeds. Judd (1901) and Nolan et al. (2002)
noted the importance of Ambrosia and Amaranthus to dark-eyed juncos.

438

THE TEXAS JOURNAL OF SCIENCE-VOL. 56(4), 2004

Martin et al. (1951) also found seeds of Ambrosia and various grasses
to be important food items for the species.

White-throated sparrows were abundant on both study areas during
winter 1982-83. With data from study areas pooled, Ambrosia , (43%)
comprised a higher proportion of that species diet than did any genera
in diets of the other species. Falls & Kopachena (1994) noted the
importance of Ambrosia to white- throated sparrows. However, they also
stated that fruits of Rhus were important to the species. During this
study, numerous white- throated sparrows were observed foraging in
Rhus , and it was assumed that they were eating Rhus fruit. Several of
those were birds were collected, yet Rhus seeds comprised a very minor
proportion of the diet. Halls (1977) noted that birds cannot sustain
weight on a heavy diet of Rhus and that it is normally eaten with other
foods. The very small amount of Rhus consumed by birds collected in
this study support Halls’ comments and indicate that birds observed
foraging in Rhus were either seeking other food items or were consum¬
ing minute quantities of that genus.

Conclusions

In this study, each bird species consumed seeds of several genera in
excess of availability. Also, availability percentages exceeded consump¬
tion percentages for some genera and did not differ for others. Al¬
though seeds of all genera were available to each species, the differences
among species may have been due to differences in habitat selection
within the clearcuts. Virtually all northern cardinals were first observed
in or adjacent to the relatively dense vegetation of the windrows or small
riparian zones which were present on both study areas. Song sparrows
were usually in dense grassy areas between rows of planted pine seed¬
lings. Dark-eyed juncos were in similar areas, but at higher elevations
where ground cover was less dense. White-throated sparrows were
collected in areas similar to those of northern cardinals. These results
demonstrate that when properly administered, the cl earcutting method of
regeneration creates excellent habitat for ground- foraging, seed-eating
birds which winter in the southern United States. This method creates
openings in the forest and, combined with site preparation techniques
that scarify both the soil and dormant seeds, promotes the establishment
of seed-bearing forbs and grasses.

WORTHINGTON, WHITING & DICKSON

439

Acknowledgments

We appreciate the field assistance of Steve Best and Nolan Smith and
the laboratory assistance of Tracy Flavins, Kathleen Kroll, and Karen
Hoza- Wilson. We are indebted to John Roese for much of the statistical
analyses. Rhonda Barnwell, Crystal Linebarger, and Ashley Sample
provided manuscript preparation. This project was funded by the U.S.
Forest Service, Southern Experiment Station, and the Arthur Temple
College of Forestry at Stephen F. Austin State University.

Literature Cited

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Dillery, D. G. 1965. Post-mortem digestion of stomach contents in the savannah sparrow.
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Falls, J. B. & J. G. Kopachena. 1994. White-throated sparrow. In The birds of North
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Handbook No. 219, 171 pp.

Nolan, V., Jr., E. D. Ketterson, D. A. Cristol, C. M. Rogers, E. D. Clotfelter, R. C. Titus,
S. J. Schoech & E. Snajdr. 2002. Dark-eyed junco. In The birds of North America,
No. 716 (A. Pool and F. Gill, editors). The Academy of Natural Sciences, Philadelphia,
Pennsylvania and the American Ornithologists’ Union, Washington, D.C., pp. 1-42.

440

THE TEXAS JOURNAL OF SCIENCE-VOL. 56(4), 2004

West, G. C. 1973. Foods eaten by tree sparrows in relation to availability during summer
in northern Manitoba. J. Arctic Institute of North Am., 26(1):7-21.

Worthington, D. W. 1984. Winter songbird feeding habits on east Texas clearcuts.
Unpublished M.S. thesis, Stephen F. Austin State University, Nacogdoches, Texas, 83

pp.

RMW at: mwhiting@sfasu.edu

TEXAS J. SCI. 56(4):44 1-451

NOVEMBER, 2004

INDEX TO VOLUME 56 (2004)

THE TEXAS JOURNAL OF SCIENCE

Sandra L. Woods

Department of Biology, Angelo State University
San Angelo, Texas 76909

This index has separate subject and author sections. Words,
phrases, locations, proper names and the scientific names of
organisms are followed by the initial page number of the article in
which they appeared. The author index includes the names of all
authors followed by the initial page number of their respective
article(s).

SUBJECT INDEX

Abiotic Factors 35
Abiotic stress 335
Acacia berlandieri 253
Acacia farnesiana 253
Acacia rigidula 253
Acacia schaffheri 253
Acari 369
Accuracy 149
Acid Sulfate conditions 91
Activity patterns 383
Adult foraging behavior 141
Acheta domesticus 141
Allelopathic component 3
Ambrosia 427

American beech, decline in 285
American Fisheries Society 63
American Ornithologists’ Union 1957,
1998 77

Amistad Reservoir 223, 237

Aquilla Lake 187
Araneida 369
Arboreal behavior 395
Aristida 427
Arizona 267
Arkansas 73, 273
Arsenic 91
Artesia Wells 237
Arthropod assemblage 369
Asexual reproduction 175
Aspidoscelis gulaxis 237
Aspidoscelis laredoensis 237
Asteraceae 15
Asymmetrical
Avifauna 197
Axis movement 149

Baird’s pocket gophers 383
Big Thicket National Preserve 299

442

THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 4, 2004

Big Thicket Science Conference 281

Biomass 175

Bivalvia 63, 223

Brackish marshes 103

Branch elongation 253

Brittle Star 175

Broadcasting 231

Burning regime 405

Brush-Grassland 15

Burrows 383

Caenidae 123
Caenis latipennis 123
California 55
Callicarpa All
Canopy 35

Cardinalis cardinalis All

Carolina Chickadee 187

Cartago Province 81

Catarina 237

Caudata 273

Channel Islands 175

Chapparal Wildlife Management Area

Chinese tallow tree 335, 357, 369

Chloraleucon ebano 253

Clearcuts 427

Clonal complex 237

Clutch size 81

Cnemidophus gularis 237

Cnemidophorus laredoenss 237

Coahuila 223

Coastal-marshes 15

Coelomocytes 175

Coffee Snake 81

Colonized 157

Colorado River 223

Colubridae 267, 383

Commercial dog and cat chow 141

Community similarity 103
Continental shelf 157
Cooke County 73
Costa Rica 81
Crickets 141

Critical Thermal Maximum 123
Crotalus horridus 395
Crotalus cerastes 55
Croton All
Cupressacae 3

Dallas county 73
Dark-eyed j uncos 427
Datura All

Demographics of occupancy 131
Density 187

Departure from neutrality 157

Devils River 223

Diel activity patterns 383

Diet 77

Diptera 369

Diversity 187

131 Dominant species 103
Dry oak-pine forest 299
Dryocopus pileatus 415
Durophagus shark 215

Early olfactory experience 141
Eastern wild turkeys 405
Echinodermata 175
Ecological resistance 237
Ecological notes 263
Edwards Plateau 35
Emberizidae 77
Encinal 237

INDEX

443

Endoparasites 273
Ephemeroptera 123
Equal sex ratio 131
Eragrostris 427
Europe 263
Eurymerodesmidae 73
Eurymerodesmus mundus 73
Eurymerodesmus angularis 73
Evolutionary lineage 273

Fabaceae 15
Fagus grandifolia 285
Falcon Reservoir 223
Fall 197, 253

Feeding habits of songbirds 427
Feeding regimes 141
Fertilization 357
Fire 299, 319, 415
Fissiparous species 175
Flood plain 267
Flood plain forests 335
Florida 73, 263
Follicles 268

Food-borne olfactory cues 141
Forbes 427
Fossil record 215
Freshwater mussels 63
Freshwater marshes 103
Fuel characteristics 319
Full-factorial experiment 149
Fungi 415

Fusconaia askewi 63

Galactia 427
Galapagos Islands 175
Genetic drift 157

Genetic polymorphism 157
Geographic shift 179
Germination rates 347
Glacial retreat 157
Gober Chalk 215
Grasses 427

Grasshopper Mouse 141
Grayson county 73
Growth 335
Gulf of Mexico 237

Haplotype variation 157
Hardin County, Texas 285
Hemoglobin 175
Hemiptera 369

Herbaceous ground cover 405
Herbicide 347
Heterodon nasicus 267
Histological examination 268
Hogna carolinensis 141
Holotype 215
Homogeneity 157
Honduras 81
Hornshell 223
Hurricane damage 285
Hybridization 237

Illinois 73, 267
Impoundment 187
Impoverished diet 141
Incubation 207
Independent variables 149
Insect fauna 369
Intercanopy 35
Invasion 299, 335

444

THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 4, 2004

Johnson county 73
Junco hyemalis 427
Junior synonym 215
Juniperus ashei 3, 35

Kansas 215, 268
Keystone species 415
Known prey odor 141

Lakes 91

Lampsilis satura 63
Late cretanaceous 215
Limnodrilus 263
Linear model 149
Liquidambar styraciflua 357
Longleaf pine 319
Louisiana 73, 265
Louisiana pine snake 383
Lower Rio Grande Valley 253
Lutjanus campechanus 157

Macleod & Slaughter 215
Mate guarding 207
Mayfly 123
Mealworms 141
Mean error 1,49
Mearns 141

Median intrapair distance 207
Meleagris gallopavo sylvestris 405
Melospiza melodia 427
Mesic species 299, 319

Mexico 197, 223, 237, 267
Middens 131
Milliped 73
Mimus polyglottos 207
Mismatch distribution 157
Mississippi 73
Missouri 73

Mitochondrial DNA 157
Mockingbird 207
Monogamous passerine 207
Monotypic genus 73
Mudstone 91
Mulch depth 347
Muridae 131, 141
Mutation 157

Mycorrhizal fungi, inoculum 357

Native trees 335
Nebraska 73

Neches River Estuary 265
Neotoma micropus 131
Nest building 207
Nesting attempts 179
Nesting habitat 405
Neuroptera 369
Nevada 197
Nicaragua 81
Ninia maculate 8 1
North America 263
North American Rattlesnake 55
North Carolina 73, 263
Northern cardinal 187, 427
Northern Gulf of Mexico 157
Northern Mockingbird 207
Novel prey odors 141
Novel pure chemical odor 141
Nucleotide-site 157

INDEX

445

Nuevo Leon 197
Nyssa sylvatica 357

Oak 197
Oak forrest 197
Obovaria jacksoniana 63
Odor choice test 141
Odor preferences 141
Oklahoma 73, 273
Olfactory imprinting 141
Oligochaeta 263
Onychomys arenicola 141
Open Woodland 267
Ophiactis simplex 175
Ophiuroidea 175
Ortheroptera 369
Oxidation 91

Oxygen concentrations 123

PABNHS 15
pH 123

Panama 77, 81, 175

Panicum 427

Parabloids 231

Parietaria 427

Parthenogenetic 237

Passeriformes 77

Paternity assurance behavior 207

Payload 149

Peloscolex 263

Peripheral populations 237

Periplaneta americana 141

Physiological Tolerance ranges 123

Picoides borealis 415

Pileated woodpeckers 415

Pine 197

Pine oak 197
Pine snake 383

Pineywoods Ecological Region 405

Pirns palustris 319

Pinus taeda 357

Pituophis ruthveni 383

Plethodon glutinous 273

Plethodontidae 273

Plethodon Sequoyah 273

Pleurobema riddellii 63

Poecile caroinensis 187

Poaceae 15

Polydesmida 73

Popenaias popeii 223

Postal notice 455

Prairie 267

Prairie restoration 347
Precipitated Fe(OH)3 91
Prescribed fire 319
Ptychodontidae 215
Ptychodus martini Williston 215
Ptychodus connellyi 215
Pyrite 91

Quadrula mortoni 63
Quercus alba 357
Quercus nigra 357

Radars 231
Radio-telemetry 383
Rainfall 253

Radial error variability 149
Radio- marked 405
Random component 149
Rasacas 15

446

THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 4, 2004

Rat snakes 415

Red-cockaded woodpecker 415
Red Snapper 157
Red tube feet 175
Regressed testes 55
Regression model 149
Repeatability 149
Reproduction 81, 171
Reproductive cycle 268
Reproductive data 268
Reservoirs 91

Reservoirs impoundment 187

Revolution 231

Rio Grande 73, 237

Rio Grande Delta 103

Rio Grande Valley 77, 179

Rio Sabinas 223

River centered zone 237

Roaches 141

Robotics 149

Roden tia 131, 141

Roxton Limestone member 215

Salamander 273

Salt flats 15

Salt marshes 103

San Luis Potosf 267

Sandy substrate 237

Sapium sebiferum 335, 357, 369

Sapling growth and mortality 299

Savannah restoration 347

Searching behavior 141

Secondary vilellogensis sensu 268

Sediments 91

Seed germination 347

Seedlings 3

Seedling demography 35
Seeds 427

Semidester habitat 268
Serpentes 267

Sequoyah slimy salamander 273
Serpentes 81
Seteria 427

Sevier County, Arkansas 273
Shade- tolerant species 299
Shannon’s Diversity Index 197
Shredding mowers 347
Single breeding season 179
Snags 415
Snake 268
Social structure 131
Soil fertility 357
Solar energy collection 23 1
Songbirds, feeding habits 427
Song sparrows 427
South Concho River 223
Southern Canada 267
Southern mixed forests 285
Southern Plains Woodrat 131
Species composition 103
Species diversity 103
Species evenness 103
Species richness 103, 369
Speed 149

Sporophila torqueola 77
Spring 197, 253
Squamata 237
Standard deviation 149
Stem density 319
Stepwise fluctuations 123
Structural changes 319
Summer 197
Sulfur 91
Survivorship 123
Syntopy 237
Systematic 263

INDEX

Tamaulipas State, Mexico 237
Tanyard Branch Creek 123
Tanks 15

Taught position 149
Taxonomic 263
Teeth 215
Teiidae 237
Telemetry studies 395
Temporal signature 157
Temperature 347
Tenebrio molitor 141
Terrestrial avian communities 187
Testicular cycle 55
Texas 15, 73, 77, 91, 131, 175, 179,
215, 223, 237, 263, 253
Texas Counties:

Cameron 15
Cooke 73
Dallas 73
Dimmit 237
Fannin 215
Grayson 73
Hardin 285
Hildago 237, 253
Johnson 73
Lasalle 237
Starr 237, 253
Walker 123
Webb 237
Zapata 237
Texas Ebony 253
Thorn scrub vegetation 237
Thysanoptera
Timber rattlesnake 395
Trans-Pecos 179
Tree litter 3
Trophic structure 369
Tubificidae 263
Tubificoides heterochaetus 263

United States 73
Unionidae 63, 223
Uplland communities 319
Upper Lower Campanian 215

Vasa deferentia 55
Vascular plants 15
Vegetational communities 197
Vermiculite Control 3
Village Creek basin 63
Viola 427

187, Virginia 263

Walker County 123
Water quality tolerance 263
Water regines, varying 335
Waves 231

Weches Formation 91
Western hognose snake 267
Western interior sea 215
White-collared seedeater 77
White-throated sparrows 427
White- winged dove 179
Wier Woods, Texas 285
Winter 197, 253, 427
Wolf Spider 141
Woodland overstory 35
Woody plant communities 319
Woody shrubs 427
Wright-Fisher model 157

Y-maze olfactometer 141
Yolk deposition 55, 268

448

THE TEXAS JOURNAL OF SCIENCE-VOL. 56, NO. 4, 2004

Zaragoza 197
Zenaida asiatica 179
Zonotrichia albicollis All

INDEX

449

AUTHOR INDEX

Amir-Moez, A. R. 231

Baccus, J. T. 179
Barker, C.A. 91
Bodily, R. Y. 207
Bordelon, V. L. 63
Bradley, R. D. 131
Brink, J. 149
Burridge, C. P. 157
Bursey, C. R. 273
Butterfield, B. J. 335

Christensen, A. B. 175
Cook, J. L. 123
Conner, R. N. 395, 415
Contreras-Balderas, A. J. 197
Cordes, J. E. 237
Correa-Sandoval, A. 223

DeWalt, S. 369
Dickson, J. G. 427
Donahue, C. 347

Ealy, M. J. 383
Eddy, M. R. 253
Eichler, B. G. 405
Eitniear, J. C. 77
Elsik, I. S. 285

Fleet, R. R. 383
Fulhorst, C. F. 131
Fulton, M. R. 285, 299

Gold, J. R. 157

Goldberg, S. R. 55, 81, 171, 267
Gonzalez-Rojas, J. I. 197

Hall, R. W. 299
Hamm, S. A. 215

Haney, A. 149

Harcombe, P. A. 285, 299, 319
Harrel, R. C. 63, 263
Hartley, M. K. 369
Hinds, B. 149
Howells, R. G. 223

Jha, S. 285

Judd, F. W. 103, 253

Judy, K. 91

Kerstupp, A. O. 197
Knox, R. G. 319

Ledger, E. B. 91
Lin, J. 299
Liu, C. 319
Lonard, R. I. 15, 103

McAllister, C. T. 73, 273
McKinley, D. 3
Moore, D. I. 73

Neudorf, D. L. H. 207
Nijjer, S. 357

Olalia- Kerstupp, A. 197

Paulissen, M. A. 237
Puckett, R. T. 123
Punzo, F. 141

Ransom, Jr., D. 187

Richard, N. L. 15

Richardson, A. T. 15

Rogers, W. E. 335, 347, 357, 369

Rudolph, D. C. 383, 395, 415

Ruthven, III, D. C. 131

Ruvalcuba-Ortega, I. 197

450

THE TEXAS JOURNAL OF SCIENCE— VOL. 56, NO. 4, 2004

Saenz, D. 395, 415

Schaefer, R. R. 395

Schaefer, C. L. 179

Shelley, R. M. 73

Shimada, K. 215

Siemann, E. 335, 347, 357, 369

Slack, R. D. 187

Small, M. F. 179

Strenth, N. E. 223

Suchecki, J. R. 131

Van Auken, O. W. 3, 35

Walker, J. M. 237
Wayne, R. 35
Welch, R. D. 179
Whiting, Jr., R. M. 405, 427
Worthington, D. W. 427

INDEX

451

REVIEWERS

The Editorial staff wishes to acknowledge the following indi-
iduals for serving as reviewers for those manuscripts considered for
publication in Volume 56. Without your assistance it would not be
possible to maintain the quality of research results published in this
volume of the Texas Journal of Science.

Abbott, J.
Allison, T.
Anderson, J.
Arnold, K.
Baskin, J.
Bestgen, K.
Bidwell, T.
Bray, S
Breshears, D.
Brush, T.
Bryan, Jr, A.
Burk, J.
Cameron, G.
Cecil, D.
Ciccimuri, D.
Clark, W.
Connor, W.
Cook, T.
Curran, S.
Dinsmore, S.
Divine, D.
Ernst, C.
Everitt, J.
Farrish, K.
Foster, C.
Gelwick, F.
Graves, J.
Harcombe, P.

Harper, C.
Harper, D.
Harrel, R.
Harveson, L.
Hathcock, C.
Henke, S.
Henry, B.
Hicks, D.
Highton, R.
Holley, A.
Howells, R.
Hurst, G.
Jones, R.

Judd, F.

Jurena, P.
Krauss, K.
Lonard, R.
MacFadden, B.
Mathewson, C.
Maxwell, T.
McAllister, C.
McDonald, H.
McGregor, K.
Monfredo, W.
Montagna, P.
Murray, H.
Nieland, D.
Norwine, J.
Ortego, B.

Painter, C.
Parker, W.
Persans, M.
Rayor, L.
Ribble, D.
Richardson, A.
Riskind, D.
Robertson, P.
Rupert, J.
Schmidlin, T.
Schwertner, T.
Schwimmer, D.
Siemann, E.
Singer, F.
Smeins, F.
Smith, E.
Stangl, Jr., F.
Taylor, E.
Upton, S.

Wake, D.
Walker, E.
Wallace, M.
Walley, H.
Welbourn, W.
Winne, C.
Wittrock, D.
Woodin, M
Zaidan, F.

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DIRECTORS

2002 Sushma Krishnamurthy, Texas A&M International University
Raymond D. Mathews, Jr., Texas Water Development Board

2003 Hudson R. DeYoe, University of Texas-Pan American
Cynthia Contreras, Texas Parks and Wildlife Department

2004 Benjamin A. Pierce, Baylor University

Donald L. Koehler, Balcones Canyonlands Preserve Program

SECTIONAL CHAIRPERSONS

Anthropology : Roy B. Brown, Institute Nacional de Antropologia y Historia
Biological Science : Francis R. Horne, Texas State University
Botany : Herbert D. Grover, Harden-Simmons University
Chemistry: Mary Kipecki-Fjetland, St. Edward’s University
Computer Science: Laura J. Baker, St. Edwards University

Conservation and Management: Felipe Chavez-Ramirez, Platte River Whooping Crane Trust

Environmental Science: William Thomann, University of the Incarnate Word

Freshwater and Marine Science: Sharon Conry, Baylor University

Geology and Geography: Carol Thompson, Tarleton State University

Mathematics: Hueytzen J. Wu, Texas A&M University-Kingsville

Physics: David Bixler, Angelo State University

Science Education: Jimmy Hand, Austin, Texas

Systematics and Evolutionary Biology: Kathryn Perez, University of Alabama

Terrestrial Ecology: Jerry Cook, Sam Houston State University

Threatened or Endangered Species: Alice L. Hempel, Texas A&M University-Kingsville

COUNSELORS

Collegiate Academy: William J. Quinn, St. Edward’s University
Junior Academy: Vince Schielack, Texas A&M University
Nancy Magnussen, Texas A&M University

THE TEXAS JOURNAL OF SCIENCE
PrinTech, Box 43151
Lubbock, Texas 79409-3151

PERIODICAL POSTAGE
PAID AT LUBBOCK
TEXAS 79402

RETURN SERVICE REQUESTED

6543

SMITHSONIAN INSTITUTION LIBRARIES

NHB25MRC154

PO BOX 37012

WASHINGTON, DC 20013-7012

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